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SYNTHESIS and PHYLOGENETIC COMPARATIVE ANALYSES of the CAUSES and CONSEQUENCES of KARYOTYPE EVOLUTION in ARTHROPODS by HEATH B

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SYNTHESIS and PHYLOGENETIC COMPARATIVE ANALYSES of the CAUSES and CONSEQUENCES of KARYOTYPE EVOLUTION in ARTHROPODS by HEATH B SYNTHESIS AND PHYLOGENETIC COMPARATIVE ANALYSES OF THE CAUSES AND CONSEQUENCES OF KARYOTYPE EVOLUTION IN ARTHROPODS by HEATH BLACKMON Presented to the Faculty of the Graduate School of The University of Texas at Arlington in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY THE UNIVERSITY OF TEXAS AT ARLINGTON May 2015 Copyright © by Heath Blackmon 2015 All Rights Reserved ii Acknowledgements I owe a great debt of gratitude to my advisor professor Jeffery Demuth. The example that he has set has shaped the type of scientist that I strive to be. Jeff has given me tremendous intelectual freedom to develop my own research interests and has been a source of sage advice both scientific and personal. I also appreciate the guidance, insight, and encouragement of professors Esther Betrán, Paul Chippindale, John Fondon, and Matthew Fujita. I have been fortunate to have an extended group of collaborators including professors Doris Bachtrog, Nate Hardy, Mark Kirkpatrick, Laura Ross, and members of the Tree of Sex Consortium who have provided opportunities and encouragement over the last five years. Three chapters of this dissertation were the result of collaborative work. My collaborators on Chapter 1 were Laura Ross and Doris Bachtrog; both were involved in data collection and writing. My collaborators for Chapters 4 and 5 were Laura Ross (data collection, analysis, and writing) and Nate Hardy (tree inference and writing). I am also grateful for the group of graduate students that have helped me in this phase of my education. I was fortunate to share an office for four years with Eric Watson. He helped build my appreciation for the work of early evolutionary biologists and was always willing to listen to me talk about comparative methods or beetle natural history. I also benefited greatly from my interactions with other graduate students. Richard Adams, Daren Card, Nicholas Long, James McQuillan, Matthew Mosley, Jacobo Reyes- Velasco, David Sanchez, and Drew Schield have become good friends and scientists that I respect. My interest in biology began early and was nurtured by my parents and William Voss the former curator of the Fort Worth Museum of Science and History. While my parents were not particularly fond of the animals I brought home they always encouraged iii my pursuits without hesitation. I also owe thanks to Matthew Flechter who was my constant companion in collecting and studying every creature we could find. Most importantly, I owe a most heartfelt thank you to my children Abbigail and Leslie. They both have spent many hours in coffee shops, labs, offices, and the field as I worked on the research contained in this dissertation. They have been understanding, encouaraging and a source of my desire to excel. February 20, 2015 iv Abstract SYNTHESIS AND PHYLOGENETIC COMPARATIVE ANALYSES OF THE CAUSES AND CONSEQUENCES OF KARYOTYPE EVOLUTION IN ARTHROPODS Heath Blackmon, PhD The University of Texas at Arlington, 2015 Supervising Professor: Jeffery P. Demuth Cytogenetic data in the form of karyotypes are complex, highly-variable traits that offer opportunities to detect changes in genome organization, uncover phylogenetic history, and distinguish cryptic species. However, the synthesis of cytogenetic data across large taxonomic scales has been rare. Here I report the insights gained through a synthesis of all available karyotype data from Arthropoda. The first chapter focuses on two databases that were built to make these data openly available, and broad insights into the evolution of sex determination and chromosome number in Arthropoda that the collected data have made possible. This is followed by four chapters that use these data to address fundamental questions in evolutionary biology. In chapter two I address the question, why do some clades frequently lose Y chromosomes while they are rarely lost in others? I propose the fragile Y hypothesis that suggests meiotic mechanisms are of central importance in explaining the phylogenetic distribution of Y chromosome loss. In chapter three I address the question, why do some clades exhibit near stasis in chromosome number while closely related clades show great variation? Using data from beetles in a comparative framework I show that when species evolve traits that reduce effective population size v rates of chromosome number evolution increase dramatically suggesting that observed differences in chromosome number are underdominant while segregating and are fixed through random drift in small populations. In chapter four I address the question, does low chromosome number increase the probability of evolving haplodiploidy? I develop a novel comparative method to test this long-standing hypothesis first proposed by Bull (1983). The results indicate that low chromosome number increases the probability of transitions to haplodiploidy. In chapter five I address the question, do eusocial Hymenoptera have higher chromosome number than solitary Hymenoptera? Using a larger dataset than previous studies, I show that there is no support for an absolute difference in chromosome number of solitary and eusocial Hymenoptera. Instead, I find that eusocial Hymenoptera have much higher rates of chromosome evolution when compared to their solitary relatives suggesting variable selection pressure or reduced effective population size in eusocial hymenoptera. As a body of work these analyses illustrate that chromosome number and meiotic mechanisms can impact the evolution of sex determination systems and that the evolution of chromosome number is often strongly influenced by the traits an organism exhibits. vi Table of Contents Acknowledgements .............................................................................................................iii Abstract ............................................................................................................................... v List of Illustrations .............................................................................................................. xi List of Tables ......................................................................................................................xii Chapter 1 Synthesis of cytogenetic data in Insecta. ........................................................... 1 Abstract ........................................................................................................................... 1 Introduction ..................................................................................................................... 1 Methods .......................................................................................................................... 3 Results ............................................................................................................................ 5 Order summaries ........................................................................................................ 5 Chromosome number ............................................................................................... 17 Sex chromosome systems in insects ....................................................................... 19 Male and female heterogamety ................................................................................ 20 Sex-limited chromosome evolution .......................................................................... 21 Complex sex chromosomes ..................................................................................... 24 Haplodiploidy ............................................................................................................ 24 Parthenogenesis ....................................................................................................... 25 Conclusions .............................................................................................................. 26 Chapter 2 Estimating tempo and mode of Y chromosome turnover: explaining Y chromosome loss with the fragile Y hypothesis ........................................... 27 Abstract ......................................................................................................................... 27 Introduction ................................................................................................................... 28 Forces promoting Y(W)-chromosome degeneration ................................................ 30 Forces promoting Y(W)-chromosome retention ....................................................... 30 vii Methods ........................................................................................................................ 32 Data collection .......................................................................................................... 32 Comparative analysis ............................................................................................... 37 Results .......................................................................................................................... 40 Discussion .................................................................................................................... 48 Conclusion .................................................................................................................... 53 Chapter 3 Assessing the impact of key ecological and phenotypic transitions on the rate of karyotype evolution: drift drives the evolution of chromosome number. ............................................................................................................................
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