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EVOLUTIONARY GENOMICS FROM ONTOGENY TO PHYLOGENY EVOLUTIONARY GENOMICS FROM ONTOGENY TO PHYLOGENY By CARLO G. ARTIERI, B.Sc., M.Sc. A Thesis Submitted to the School of Graduate Studies in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy McMaster University © Copyright by Carlo Artieri, June 2009 DOCTOR OF PHILOSOPHY (2009) McMASTER UNIVERSITY (Biology) Hamilton, Ontario TITLE: Evolutionary Genomics from Ontogeny to Phylogeny AUTHOR: Carlo G. Artieri, B.Sc. (Dalhousie University, Halifax, Nova Scotia), M.Sc. (Simon Fraser University, Burnaby, British Columbia) SUPERVISOR: Professor Rama S. Singh NUMBER OF PAGES: [xii], 173 ii ABSTRACT Much speculation has been made about the relative importance of changes in developmental regulation of gene expression in determining major phylogenetic patterns observed both in extant and extinct species. However, most of these hypotheses have been formulated based on data obtained from the comparison of very distantly related organisms (e.g., between animal phyla). Another approach to answering questions about development (ontogeny) in the context of evolution (phylogeny) is to observe how developmental patterns diverge between closely related species, in order to obtain a better understanding of the population level processes underlying phyletic change. With the intent of addressing this possibility, the principle work outlined in this thesis investigated patterns of divergence between closely related species of Drosophila at the level of both the nucleotide coding sequence as well as gene expression levels in the context of ontogeny. The results show that the stage during which genes are expressed has a significant impact on their patterns of divergence, acting both to constrain (earlier stages) and accelerate (later stages) their rates of evolution - the latter being largely the result of sexual selection pressure. However, we also find that intermediate stages of fly development, such as metamorphosis, may experience a greater degree of conservation of the elements regulating gene expression than other stages. Nonetheless, we do find evidence that both gene expression and coding sequences may be subject to similar selection pressures, yet there also appears to be substantial uncoupling of the two, as evidenced by our observation of stage-specific, autonomous patterns of hybrid misexpression manifested in interspecific hybrids. The data presented herein shed new light on patterns of divergence between species, specifically with regards to how various selection pressures affect different stages of ontogeny. iii ACKNOWLEDGEMENTS John Dewey (1859-1952), American philosopher, psychologist, educational reformer, and lapsed Haeckelian, held views much in line with W.B. Yeats' old aphorism about likening education to the lighting of a fire, rather than the filling a bucket, when he wrote: "Knowledge," in the sense of information, means the working capital, the indispensable resources, of further inquiry; of finding out, or learning, more things. Frequently it is treated as an end in itself, and then the goal becomes to heap it up and display it when called for. This static, cold-storage ideal of knowledge is inimical to educative development. It not only lets occasions for thinking go unused, but it swamps thinking. No one could construct a house on ground cluttered with miscellaneous junk. Pupils who have stored their "minds" with all kinds of material which they have never put to intellectual uses are sure to be hampered when they try to think. They have no practice in selecting what is appropriate, and no criterion to go by; everything is on the same dead static level." -John Dewey, Democracy and Education ( 1916) I can think of no quotation that more fittingly describes the contributions to my personal development made by my supervisor, Dr. Rama Singh. While some students may prefer the reassurance provided by a 'full bucket', I've come to realize that Dr. Singh's philosophy of self-sufficiency (served with a healthy dose of encouragement and work-related discussion at the Phoenix Pub or Faculty Club), has provided me with the tools that I will require to continue my career in the often stressful, endlessly competitive, but ultimately rewarding field of scientific research. For such a boon, I shall remain eternally grateful. An equal amount of thanks must go to Dr. Wilfried Haerty, a former post-doctoral fellow in the Singh lab, who acted both in the capacity of a co-supervisor and a good friend. Much of the work that I've accomplished over the course of my education here at McMaster was made possible by his helpful advice and endless patience. I am also grateful to the members of the faculty of Biology who made up my supervisory committee, Drs. Brian Golding, Ana Campos, Ben Evans, and Richard Morton, for their constructive criticism and helpful advice. Science is a collaborative endeavor, and their friendly, knowledgeable aid has helped immensely. Speaking of collaborations, thanks must also go to the other members of the Singh lab, both current and former, especially Santosh Jagadeeshan and Abha Ahuja who provided both constructive criticism and helpful encouragement during all of the myriad iv challenges I faced in completing my work. Such appreciation must also be extended to my peers in graduate studies, notably Maria Abou-Chakra, David Anderson, Adam Bewick, Steven Brown, Freddy Chain, Paul Craig, Weilong Hao, Melanie (Sr.) Huntley, Melanie (Jr.) Lou, Allyson MacLean, Bart Maslikowski, Andrea Morash, Luca Poloni, Marie-Pierre Schippers, Iqbal Setiadi, and Wilson Sung. Thanks for making the department of biology such a great working environment. On the technical side, I must thank Dr. Timothy Westwood, and his technician Kaiguo Mo at the Canadian Drosophila Microarray Center for the immensity of their assistance with regards to the gene expression work that I've performed. I must also thank Dr. Grant McClelland, and again his student Paul Craig, for allowing me to use their qPCR equipment, in addition to instructing me in its proper use. I would also like to acknowledge the assistance of three excellent undergraduates: Marisa Melas, Priya Iyer, and Marek Gruca. Special thanks must be reserved for my father Emidio, my mother Joanne, my sister Nadia, and the other members of my family for their love and encouragement. And finally, most of all, to my girlfriend Julie for putting up with all of the stress that I'd occasionally bring home from the lab. Her love and support kept my 'head above the water' most of all. The dedication to my M.Sc. thesis read: "To my high-school principle, who told me that I was not 'university material'. Thank you for giving me a goal to pursue and thus the drive to succeed." I shall not break with tradition, and again dedicate my Ph.D. thesis to the same individual. As a man who dedicated his own life to education, I'm certain that he'll be happy to learn that, given the existence of this manuscript, his hypothesis about my composition likely warrants rejection. v TABLE OF CONTENTS 1 General Introduction .......................................................................... 1 1.1 Overview ........................................................................................... 1 1.2 Speciation Genetics .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. 4 1.2.1 The genetic 'problem' of speciation .......................................... 4 1.2.2 Haldane's rule ..................................................................... 10 1.2.3 The genetics of speciation in the molecular era .. .. .. .. .. .. .. .. .. .. .. .. 14 1.2.3. l Identification of 'speciation genes' ......................... 14 1.2.3.2 Sexual selection and speciation . .. .. .. .. .. .. .. .. .. 17 1.2.3 .3 Studies of speciation at the level of gene expression . 18 1.3 Ontogeny and Phylogeny .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. 22 1.3 .1 Development in the context of evolution .. .. .. .. .. .. .. .. .. .. .. .. 22 1.3.2 Von Baer's 'laws' ................................................................ 24 1.4 Aims of the Thesis .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. 27 1.5 References . .... .... .. ... ..... ....... ..... .. .... .. .. .... .. .. .. ... .. .. .. .. ... .. ... .. 30 2 Sexual Selection and Maintenance of Sex: Evidence from Comparisons of Rates of Genomic Accumulation of Mutations and Divergence of Sex-Related Genes in Sexual and Hermaphroditic Species of Caenorhabditis ................................................................... 45 2.1 Abstract . .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. 46 2.2 Introduction .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. 46 2.3 Materials and Methods .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. 48 2.4 Results .......................................................................................... 50 2.5 Discussion . .. .. .. ... .... .... .. ... ... ... .. ..... .............. ... .. .. .. ....... .... .. .. .. .. .. 53 vi 2.6 References .. ... .. .. ... .... .. ......... .. .. .. .. .. .. ........ .. .. .. .. .. .. ...... ..... ... .... ... 58 3 Association Between Levels of Coding Sequence Divergence and Gene Misregulation in Drosophila Male Hybrids ........................... 67 3 .1 Abstract . 68 3 .2 Introduction . 68 3.3 Materials and Methods ....................................................................
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