ptg Praise for Evolution: A View from the 21st Century “A novel description of evolution based on modern genetic analysis is presented in detail. Shapiro has written a stimulating, innovative manuscript that surely Darwin would have liked.” —Sidney Altman, Yale University; Nobel Laureate in Chemistry, 1989 “Based on a long and highly competent personal experience in science and his novel insights into biological functions, the author has reached views of biological evolution that can reveal to a wide, interested readership how the living world co-evolves with the environment through its intrinsic powers.” —Werner Arber, Professor Emeritus, University of Basel, Switzerland; Nobel Laureate in Physiology/Medicine, 1978 “Professor Shapiro’s offering is the best book on basic modern biology I have ever seen. As far as I can tell, the book is a game changer.” —Carl Woese, University of Illinois; discoverer of Archaea, the third realm of life; National Medal of Science 2000 ptg “This moving, clearly written, if complex, description of ‘natural genetic engineering’ explains evolutionary processes that preceded people by at least 3,000 million years. Shapiro’s detailed account of ubiquitous genetic dynamism, DNA machination, repair, and recombination in real life, bacterial to mammalian, destroys myths. Genes, whatever they are, are not ‘eternal.’... Shapiro’s careful, authoritative narrative...is entirely scientific and should interest all of us who care about the evolution of genetic systems.” —Lynn Margulis, University of Massachusetts, Amherst; National Academy of Sciences, National Medal of Science 1999 “From revisiting the Central Dogma, to outlining a systems biological approach to evolution, this book is a magnificent analysis of the key questions of the origin of variation and, therefore, of evolutionary change. Starting from his early encounter with the work and ideas of Barbara McClintock, through to his work on systems engineering as the key to understanding organisms, Jim Shapiro has new insights on all the central issues of evolutionary theory. The genome becomes a read-write storage system rather than the sole determinant of heredity. After reading this book, you will find it imperative to see biology as the 21st century is coming to see it. The ambitious title of the book is fully justified. This book gives solid biological evidence on the origin of variation and evolutionary change. That evidence will surprise those who still think that variation is random. Cells and organisms sense their environment and transmit that information to their genomes. Brilliant.” —Denis Noble, CBE FRS, Balliol College, Oxford; author of The Music of Life “Evolution, or constant change in nature, is the deepest of human ideas. It is the core of all physical, biological, and social systems and sciences—linking energy, matter, life, and consciousness. The dramatic genomic revolution unfolded new informative horizons of constant combinatorial diversity, change, and emerging innovation from simple to complex in biological evolution. Much of the understanding of genome complex adaptive architecture, dynamic reorganization, expression, and regulation—as well as the origin of life, cells, and biochemical networks—is a future challenge. This book highlights the exciting challenges to explore future nonconventional and nondogmatic vistas of evolutionary biology. The explorative mysteries include roles in evolution of nonrandom adaptive mutations, epigenetics, and repetitive DNA function and regulation. All contribute to dynamic systems biology and engineering between the evolving genome, cell, and environmental stresses and changes affecting the dynamic genome read-write memory system underlying life’s evolution.” —Eviatar Nevo, University of Haifa, U.S. National Academy of Sciences; explorer of Evolution Canyon ptg Evolution A View from the 21st Century James A. Shapiro ptg Vice President, Publisher: Tim Moore Associate Publisher and Director of Marketing: Amy Neidlinger Acquisitions Editor: Kirk Jensen Editorial Assistant: Pamela Boland Development Editor: Russ Hall Senior Marketing Manager: Julie Phifer Assistant Marketing Manager: Megan Colvin Cover Designer: Chuti Prasertsith Managing Editor: Kristy Hart Project Editor: Anne Goebel Copy Editor: Gayle Johnson Proofreader: Linda Seifert Indexer: Erika Millen Senior Compositor: Gloria Schurick Manufacturing Buyer: Dan Uhrig ©2011 by James A. Shapiro Publishing as FT Press Science Upper Saddle River, New Jersey 07458 FT Press Science offers excellent discounts on this book when ordered in quantity for bulk purchases or special sales. For more information, please contact U.S. Corporate and Government Sales, 1-800-382-3419, [email protected]. For sales outside the U.S., please contact International Sales at [email protected]. Company and product names mentioned herein are the trademarks or registered trademarks of their respective owners. ptg All rights reserved. No part of this book may be reproduced, in any form or by any means, without permission in writing from the publisher. Printed in the United States of America First Printing June 2011 ISBN-10: 0-13-278093-3 ISBN-13: 978-0-13-278093-3 Pearson Education LTD. Pearson Education Australia PTY, Limited Pearson Education Singapore, Pte. Ltd. Pearson Education Asia, Ltd. Pearson Education Canada, Ltd. Pearson Educación de Mexico, S.A. de C.V. Pearson Education—Japan Pearson Education Malaysia, Pte. Ltd. Library of Congress Cataloging-in-Publication Data: Shapiro, James Alan, 1943- Evolution : a view from the 21st century / James A. Shapiro. p. cm. ISBN 978-0-13-278093-3 (hardback : alk. paper) 1. Evolution (Biology) 2. Genomics. 3. Molecular genetics. 4. Evolutionary genetics. I. Title. QH447.S53 2012 576.8—dc22 2011008338 This book is dedicated to Felix and Gus and all future grandchildren. May their generation share nature’s deep wisdom in adapting life to its home on Earth. ptg This page intentionally left blank ptg Contents Acknowledgments . . . . . . . . . . . . . . . . . . . . . . .xiii About the Author . . . . . . . . . . . . . . . . . . . . . . . .xv A Note on Reading This Book for Individuals with Different Backgrounds . . . . . . . . . . . . . . . .xvii Introduction: Taking a Fresh Look at the Basics of Evolution in the New Century . . . . . . . . . . . . . .1 Part I Sensing,Signaling,and Decision-Making in Cell Reproduction . . . . . . . . . . . . . . . . . . . . . . .7 HowE.Coli Chooses the Best Sugar to Eat . . . . . . . . . .8 Proofreading DNA Replication . . . . . . . . . . . . . . . . . .12 DNA Damage Repair and Mutagenesis . . . . . . . . . . . .14 Cell Cycle Checkpoints . . . . . . . . . . . . . . . . . . . . . . .18 Signaling from the Cell Surface to the Genome: Pheromone Response in the Sexually Aroused Yeast Cell . . . . . . . . . . . . . . . . . . . . . . . . . . . . .21 ptg The Role of Intercellular Signals in the Cell Death Decision . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .23 Revisiting the Central Dogma of Molecular Biology . . .24 Part II The Genome as a Read-Write (RW) Storage System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .27 Genome Formatting for Proper Access to Stored Information . . . . . . . . . . . . . . . . . . . . . . . . . . . . .30 Genome Compaction,Chromatin Formatting, and Epigenetic Regulation . . . . . . . . . . . . . . . . . . .31 Genome Formatting for Replication,Localization, and Transmission to Daughter Cells . . . . . . . . . . . .36 Distinct Classes of DNA in the Genome . . . . . . . . . . .39 The Molecular Mechanisms of Natural Genetic Engineering . . . . . . . . . . . . . . . . . . . . . . . . . . . . .43 Natural Genetic Engineering as Part of the Normal Life Cycle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .55 Cellular Regulation of Natural Genetic Engineering . . .69 Targeting of Natural Genetic Engineering within the Genome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .82 Reviewing What Cells Can Do to Rewrite Their Genomes over Time . . . . . . . . . . . . . . . . . . . . . . .87 viii Evolution: A View from the 21st Century Part III Evolutionary Lessons from Molecular Genetics and Genome Sequencing . . . . . . . . . . . . . . . . .89 Antibiotic Resistance and Horizontal DNA Transfer . . .90 The Modular and Duplicative Nature of Protein Evolution . . . . . . . . . . . . . . . . . . . . . . . . .95 Molecular Taxonomy and the Discovery of a New Cell Type . . . . . . . . . . . . . . . . . . . . . . . . . . . .98 Symbiogenesis and the Origin of Eukaryotic Cells . . .100 Natural Genetic Engineering and Evolutionary Genomic Innovation . . . . . . . . . . . . . . . . . . . . . .107 Use and Reuse of Evolutionary Inventions . . . . . . . .115 What Makes a Man Different from a Mouse? . . . . . .118 Whole Genome Doubling at Critical Stages of Evolutionary Innovation and Divergence . . . . . . . .120 Reviewing What the DNA Record Reveals about Cell Activities over Evolutionary Time . . . . . . . . . .124 Part IV A New Conceptual Basis for Evolutionary Research in the 21st Century . . . . . . . . . . . . .127 A Systems Approach to Generating Functional Novelties . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .129 Reorganizing Established Functions to Generate ptg Novelty . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .130 Generation of Novel Components . . . . . . . . . . . . . .131 Retention,Duplication,and Diversification of Evolutionary Inventions . . . . . . . . . . . . . . . . . . . .133 The Implications of Targeting Genome Restructuring . . . . . . . . . . . . . . . . . . . . . . . . . . .134 Can Genomic Changes Be Linked to Ecological Disruptions? . . . . . . . . . . . . . . . . . . . . . . . . . . .139 What Might a 21st Century Theory of Evolution Look Like? . . . . . . . . . . . . . . . . . . . . . . . . . . . . .142 Where Does Evolution Fit in 21st Century Science? . . .145 Glossary . . . . . . . . . . . . . . . . . . . . . . . . . . . .149 References . . . . . . . . . . . . . . . . . . . . . . . . . .175 Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .241 Contents ix The following material can be found online only (www.ftpress.com/shapiro): Appendixes to Part I and Part II of the Printed Book Appendix I.1. Thelacoperon control circuit. Appendix I.2. S.cerevisiae pheromone response signal network (Sprague 1991). Appendix II.1. Formatting the genome for transcriptional control. Appendix II.2. Natural genetic engineering in B lymphocytes for the rapid evolution and maturation of a virtually infinite diversity of antigenbinding proteins. References Table References for Part II and Part III of the Printed Book Table II.1 DNA content in higher eukaryotes (Shapiro and Sternberg 2005) Table II.2 Different classes of annotated repetitive genome components (amplified from (Shapiro and Sternberg 2005)) Table II.3 Generic Cell Operations That Facilitate DNA Restructuring [30,61,392] Note:These references are ptg listed in the printed book only. Table II.4 Natural Genetic Engineering Systems [6-8] Note:These references are listed in the printed book only. Table II.5 Control of bacterial protein synthesis (phase variation) and modification of protein structure (antigenic variation) by natural genetic engineering (expanded from (Wisniewski-Dye and Vial 2008)) Table II.6 Applications of site-specific recombination to different functions in bacterial cells (Hallet and Sherratt 1997) Table II.7 Various stimuli documented to activate natural genetic engineering Table II.8 Genomic responses to changes in ploidy and interspecific hybridization in plants and animals Table II.9 RNA-based defense against viruses and plasmids in bacteria,archaea,fungi and plants Table II.10 Life history events that alter the epigenome (DNA methylation and chromatin formatting) Table II.11 Examples of targeted natural genetic engineering Table III.1 Examples of intercellular and interkingdom DNA transfer Table III.2 Natural genetic engineering documented in the evolution of sequenced genomes