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Evolutionary Ecology of Mammalian Placental Invasiveness

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EVOLUTIONARY ECOLOGY OF MAMMALIAN PLACENTAL INVASIVENESS Michael G. Elliot M.A., University of Oxford, 1998 THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE In the Department of Biological Sciences O Michael G. Elliot 2007 SIMON FRASER UNIVERSITY Fa11 2007 All rights reserved. This work may not be reproduced in whole or in part, by photocopy OF other means, without permission of the author. APPROVAL Name: Michael G. Elliot Degree: Master of Science Title of Thesis: Evolutionary ecology of mammalian placental invasiveness Examining Committee: Chair: Dr. R. Ydenberg, Professor Dr. B. Crespi, Professor, Senior Supervisor Department of Biological Sciences, S.F.U. Dr. A. Mooers, Associate Professor Department of Biological Sciences, S.F.U. Dr. T. Williams, Professor Department of Biological Sciences, S.F.U. Dr. J. Reynolds, Professor Department of Biological Sciences, S.F.U. Public Examiner 4 December Date Approved Declaration of Partial Copyright Licence The author, whose copyright is declared on the title page of this work, has granted to Simon Fraser University the right to lend this thesis, project or extended essay to users of the Simon Fraser University ~ibrary,and to make partial or single copies only for such users or in response to a request from the library of any other university, or other educational institution, on its own behalf or for one of its users. The author has further granted permission to Simon Fraser University to keep or make a digital copy for use in its circulating collection (currently available to the public at the 'Institutional Repositoryn link of the SFU Library website <www.lib.sfu.ca> at: <http://ir.lib.sfu.ca/handle/l892/112>) and, without changing the content, to translate the thesislproject or extended essays, if technically possible, to any medium or format for the purpose of preservation of the digital work. The author has further agreed that permission for multiple copying of this work for scholarly purposes may be granted by either the author or the Dean of Graduate Studies. It is understood that copying or publication of this work for financial gain shall not be allowed without the author's written permission. Permission for public performance, or limited permission for private scholarly use, of any multimedia materials forming part of this work, may have been granted by the author. This information may be found on the separately catalogued multimedia material and in the signed Partial Copyright Licence. While licensing SFU to permit the above uses, the author retains copyright in the thesis, project or extended essays, including the right to change the work for subsequent purposes, including editing and publishing the work in whole or in part, and licensing other parties, as the author may desire. The original Partial Copyright Licence attesting to these terms, and signed by this author, may be found in the original bound copy of this work, retained in the Simon Fraser University Archive. Simon Fraser University Library Burnaby, BC, Canada Revised: Fall 2007 ABSTRACT Eutherian mammals differ markedly in placental form and function. In species with invasive placentation the fetal epithelium of the placenta is bathed in flowing maternal blood, giving the fetus an opportunity to extract resources directly from the mother and to secrete substances which modify maternal blood chemistry. In species with non-invasive placentation the fetal tissues are separated from maternal blood by a barrier of maternal cell layers which limits the ability of the fetus to control resource transfer during gestation. My thesis explores the role played by placental invasiveness in the evolution of eutherian brain size, life history and reproductive isolation. I find that the relationships between brain size, body size and lifespan, and the rate at which hybrid inviability evolves, differ strikingly between species with invasive versus non-invasive placentation. I propose a number of physiological mechanisms that may account for such differences among eutherian mammals. Keywords: Eutheria; Placenta; Reproductive physiology; Evolution; Brain size; Life history Subject headings: Mammals - reproduction; Mammals - evolution; Reproduction - physiology; Placenta DEDICATION I dedicate this thesis to my partner, lover, intellectual sparring-partner and best friend, Sonia Memetea. Without her unfailing support and encouragement, far beyond the call of duty or reason, it would never have been possible. I would like to thank all the members of the FAB* Lab for their encouragement, and for keeping me interested with their own weird and wonderful work. I especially wish to thank Jeff Joy, Christine Parent, Rutger Vos, Patrik Nosil, Erica Jeffreys and Sampson Wu for making the Crespi lab such a pleasant and invigorating place to work. I wo~~ldlike to thank Arne Mooers for his kindness and support, and for always encouraging my computational interests. Without Marlene Nguyen's support I would long ago have drowned in a sea of unsigned forms and missed deadlines. I will always be grateful for the generosity and kindness of Livia Memetea since my arrival in Canada, and hope she is back with us soon. Finally I would like to thank Bernie Crespi. He has been a better supervisor than I could possibly have hoped for, always putting the interests of his students first and always ready with fresh insights on what seem like tired problems. His broad interests, deep knowledge and consistently crazy hypotheses have interested, entertained and educated me. TABLE OF CONTENTS .. Approval ..............................................................................................................11 ... Abstract .............................................................................................................. 111 Dedication ...........................................................................................................iv Acknowledgements ............................................................................................v Table of Contents ...............................................................................................vi ... List of Figures ..................................................................................................VIII List of Tables ......................................................................................................ix Chapter I: lntroduction ....................................................................................... The role of physiology in life history evolution ....................................................2 Evolution of brain-body allometry in mammals ..................................................4 Placentation. brain size and life history ..............................................................6 Parent-offspring conflict .................................................................................... 7 Speciation ..........................................................................................................9 Chapter 2: Divergent brain-body allometry and heterochrony between eutherian mammals with invasive versus non-invasive placentation .......................................................................................................11 Introduction ......................................................................................................11 Methods .........................................................................................................16 Results ..........................................................................................................18 Brain-body allometry ..................................................................................... 18 Encephalization quotient ..............................................................................25 Proportion of brain and body growth occurring prenatally versus postnatally .....................................................................................26 Prenatal brain growth rate ............................................................................27 Precocious and altricial young ......................................................................28 Alternative hypotheses .................................................................................30 Discussion .......................................................................................................34 Physiological mechanisms ...........................................................................34 Concluding remarks .........................................................................................40 Chapter 3: Prenatal effects on brain size evolution: life history. ecology and parent-offspring conflict .............................................................44 Introduction ...................................................................................................... 44 Materials and methods .....................................................................................49 Results ............................................................................................................52 Str~~cturalequation modelling of mammalian life history............................... 52 The slow-fast life hisory continuum............................................................... 55 Offspring quantity and quality .......................................................................57 Growth rates before and after birth ...............................................................59
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