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Proquest Dissertations Evolution of Uniparental Genetic Systems in Dermanyssine Mites (Acari: Mesostigmata) A THESIS SUBMITTED FOR THE DEGREE OF DOCTOR OF PHILOSOPHY OF THE UNIVERSITY OF LONDON by Robert Hamish Cruickshank Molecular Biology Unit, Department of Zoology, The Natural History Museum, Cromwell Road, South Kensington, LONDON SW7 5BD, England, UK Department of Biology, The Galton Laboratory, University College London, 4 Stephenson Way, LONDON NW l 2HE, England, UK September 1997 ProQuest Number: 10045787 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. uest. ProQuest 10045787 Published by ProQuest LLC(2016). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. Microform Edition © ProQuest LLC. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 DEDICATION This thesis is dedicated, with love, to my wife Alice who I met and married whilst working on this project and who has put up with so much to help me get it finished. "The meaning of this degree is that the recipient of instruction is examined for the last time in his life, and is pronounced completely full. After this, no new ideas can be imparted to him. " Stephen Leacock "Sunshine Sketches of a Little Town” ACKNOWLEDGEMENTS This thesis could not have been completed without the guidence, enthusiasm and patience of my supervisor Dr. Richard H. Thomas, who spent many hours reading manuscripts and providing a great deal of valuable advice. Many thanks are also due to Dr, James Mallet, my supervisor at UCL, not least for steering me through the bureaucracy associated with submitting a thesis. Thanks must also go to Andy Warlow and all the staff of the Molecular Biology Unit in the Department of Zoology at the Natural History Museum over the last four years, for providing such a stimulating and friendly environment in which to work. Particular thanks must go to Jackie McKenzie-Dodds, Debbie Goode and Neil Shailer. I would also like to thank all the staff of the Natural History Museum library for providing a truly remarkable collection of material to distract me from my laboratory work. I could not have done any of this work without the help of people who were willing to send me samples. They are acknowledged individually in chapter 4 but particular thanks must go to Dr. Ann Baker of the Natural History Museum, not only for providing samples herself but also for suggesting other potential sources and for identifying mites I had got from elsewhere when I know she had many more important things to do. Thanks are also due to all of the staff and participants of the Ohio State University Acarology Summer Program 1994 for an inspiring introduction to the world of mite taxonomy and also to Dr G. W. Krantz, Dr Evert E. Lindquist, Dr. Frank J. Radovsky and Dr. David E. Walter for constructive and insightful comments on my original research objectives. Financial support for this project was provided by the Biotechnology and Biological Sciences Research Council (BBSRC), formerly part of the Science and Engineering Research Council (SERC). My greatest debt of thanks, however, must go to my parents Joy and Graeme Cruickshank for a lifetime of support, encouragement and love. In many ways I still feel like a small boy turning over rotten logs and staring in wonder at all the bewildering creatures beneath. I feel very lucky to have been able to pursue this fascination into adulthood and sincerely grateful to everyone who has helped to make it happen. ABSTRACT An exhaustive survey of uniparental genetic systems (those in which at least some individuals only transmit the genome of one parent to their offspring) within the Metazoa is presented including a new scheme for the classification of such systems (chapter 1). This is followed by a critical review of 13 different hypotheses proposed to account for the evolution of these systems (chapter 2). The hypothesis of Schrader and Hughes- Schrader, originally proposed in 1931 {Q. Rev. Biol 6 : 411-438), is then introduced. This states that arrhenotoky (in which males arise from unfertilised eggs whilst females arise from fertilised eggs) evolves via an intermediate pseudoarrhenotokous stage (in which although males are produced biparentally they eliminate the genome of paternal origin at some point prior to spermatogenesis) rather than directly from a zygogenetic ancestor. The remainder of this thesis is concerned with testing this hypothesis. Criticisms of the hypothesis of Schrader and Hughes-Schrader made by Haiti and Brown in 1970 (Theor. PopuL Biol 1: 165-190) are re-examined in the light of more recent evidence and found to be invalid. Further evidence is cited from the recent literature in favour of the hypothesis of Schrader and Hughes-Schrader. A comprehensive review of the genetic systems of the Acari (mites and ticks) is used to ask whether our current state of knowledge in this field is sufficient to test the hypothesis of Schrader and Hughes- Schrader in this group. This reveals that the missing component required for such a test is a reliable hypothesis of phylogenetic relationships (chapter 3). A molecular phylogeny of the Dermanyssina (Acari: Mesostigmata) based on 755 base pairs of 28S ribosomal DNA is presented and this is shown to support the hypothesis of Schrader and Hughes-Schrader (chapters 4 and 5) A published morphological data set for the Dermanyssina is analysed and combined with the molecular data set in a variety of ways. An analysis of character conflict between the data sets is used to make an assessment of the suitability of the morphological characters for phylogenetic inference (chapter 6). Finally the hypothesis of Schrader and Hughes-Schrader is used to ask why is it always the males which are the haploid sex in haplodiploid species and ideas are presented for the future research (chapter 7). O' Contents Chapter One: Uniparental Genetic Systems and the Evolution of Haplodiploidy. I. Diversity of Uniparental Genetic Systems, Concepts and Definitions .............................................................................................................................13 SUMMARY.....................................................................................................................13 INTRODUCTION.......................................................................................................... 13 HISTORICAL PERSPECTIVE..................................................................................... 14 THE CONCEPT OF THE GENETIC SYSTEM..........................................................16 THE CONCEPT OF THE UNIPARENTAL GENETIC SYSTEM...........................16 DETERMINANTS OF UNIPARENTAL GENETIC SYSTEMS.............................17 Uniparental Genetic Systems Determined by Parental Species ............................17 Uniparental Genetic Systems Determined by Parental Sex .................................. 18 TEMPORAL SCALE IN UNIPARENTAL GENETIC SYSTEMS..........................19 The Timing of Genome Loss ...................................................................................22 Pseudogamy..............................................................................................................23 THE SEX DETERMINED UNIPARENTAL GENETIC SYSTEMS...................... 26 The Basic Sex Determined Uniparental Genetic Systems .................................... 26 The Composite Sex Determined Uniparental Genetic Systems ............................27 Unisexual Composite Systems .......................................................................... 28 Bisexual Composite Systems ............................................................................ 28 Evolution of Composite Systems ......................................................................29 THE PREFERTILISATION SYSTEMS......................................................................29 Parthenogenesis .........................................................................................................29 The Three Traditional Forms of Parthenogenesis ............................................29 Two Other Forms of Parthenogenesis ...............................................................30 Reclassification of Parthenogenesis ..................................................................30 Male Parthenogenesis ..................................................................................31 Arrhenotoky ........................................................................................... 31 Diploid Arrhenotoky ............................................................................. 33 Female Parthenogenesis .............................................................................. 33 Thelytoky ............................................................................................... 33 Anti-Arrhenotoky ...................................................................................34 Mixed Parthenogenesis ................................................................................34 Deuterotoky ............................................................................................ 34 Arrhenothelytoky ...................................................................................35
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