BIOCHEMICAL ADAPTATION This page intentionally left blank BIOCHEMICAL ADAPTATION Mechanism and Process in Physiological Evolution Peter W. Hochachka George N. Somero 1 2002 3 Oxford New York Athens Auckland Bangkok Bogota´ Buenos Aires Cape Town Chennai Dar es Salaam Dehli Florence Hong Kong Istanbul Karachi Kolkata Kuala Lumpur Madrid Melbourne Mexico City Mumbai Nairobi Paris Sa˜ o Paulo Shanghai Singapore Taipei Tokyo Toronto Warsaw and associated companies in Berlin Ibadan Copyright # 2002 by Oxford University Press Published by Oxford University Press, Inc. 198 Madison Avenue, New York, New York 10016 Oxford is a registered trademark of Oxford University Press. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording, or otherwise, without the prior permission of Oxford University Press. Library of Congress Cataloging-in-Publication Data Hochachka, Peter W. Biochemical adaptation: mechanism and process in physiological evolution / Peter W. Hochachka, George N. Somero. p. cm. Includes bibliographical references and index ISBN 0-19-511702-6; 0-19-511703-4 (pbk.) 1. Adaptation (Physiology) 2. Physiology, Comparative. 3. Molecular evolution. I. Somero, George N. II. Title. QP82.H632 2001 572.8 0 38-(cid:1)dc21 2001032142 9 8 7 6 5 4 3 2 1 Printed in the United States of America on acid-free paper Dedicated to C. Ladd Prosser and Knut Schmidt-Nielsen teachers, researchers, pathfinders, and role models This page intentionally left blank Preface The eighteen years that have elapsed since we last attempted to fit the broad field of ‘‘biochemical adaptation’’ between two covers have witnessed an explosive growth of information in virtually every area of study encompassed by our field. This statement holds whether the topic in question is metabolic regulation, protein structure–function relationships, the control of gene expression, the physics of intracellular water, or the evolutionary origin of new classes of proteins. The informa- tion explosion that students of biochemical adaptation have experienced during this period has of course been matched by equally and often more explosive growth in other biological disciplines. At the time we wrote our last volume, even optimists like ourselves would have underestimated the amount of progress that would take place in the biological sciences during the closing decades of the past century. In particular, we probably would not have foreseen that many of the questions that served as focal points of our previous volume would receive detailed answers by the time we set out on our next writing effort. Yet, as we are all aware, such progress comes with both positive and negative aspects, a kind of good news/bad news situation. Thus, the excitement that accompanies discovery of the wealth of new knowledge in biology is sometimes paired with a sense of desperation: How are we to assim- ilate all of this new detail (the proverbial ‘‘trees’’ of information) while retaining within our scientific field of vision a clear overview of the ‘‘forest,’’ that is, of the major integrative theories of our discipline? How must our existing theories be modified in the face of new data? Can entirely new conceptual syntheses now be developed on the basis of recent discoveries? How are we to deal with cross-disciplinary challenges that also abound? How do the discoveries and theories of one field impact the status of sister disciplines, ones that may lie close to the periphery of our scientific field of vision? The challenges faced in dealing with ‘‘informational’’ issues of these sorts are heightened by the fact that new experimental approaches, important new theoretical developments, and a great deal of new jargon have entered biology. These manifestations of progress frequently have the unfortunate consequence of making much of the literature seem as though it is penned in a foreign language. Can a biologist any longer read the table of contents in widely focused journals like Science and Nature and hope to comprehend what all of the articles related to ‘‘biology’’ are about? An unfortunate trend linked to progress in biology is increased specialization: Investigators find themselves feeling most comfortable and secure (and most apt to be funded) when dealing with a limited suite of phenomena and techniques. Biologists more and more frequently seem to be speaking to a restricted set of their peers, those specialists to whom they can talk their particular language. Despite the trend toward increased specialization, many biologists strive to carry out and to communicate integrative analyses that represent synthetic, cross-disciplinary contributions. In these analyses, data from many types of experimentation, performed at different levels of complex- ity in the hierarchy of biology phenomena, are incorporated into investigations of broad-scale questions. The present volume is an attempt to reach this very goal. We approached this project with the desire to integrate a wide range of information from studies of topics like the regulation of gene expression, metabolic biochemistry, protein structure–function relationships, genomics, and proteomics into a framework that would allow the reader to gain deeper understanding of broadly important issues in evolution, ecology, biodiversity, and biogeography. As the subtitle of this volume is meant to suggest, we have taken an integrative approach in two different senses of the term. First, we have attempted in each topic covered to traverse as many rungs on the reduc- tionist ladder as was possible with available information. Through these exercises we have tried to place a fundamental mechanistic foundation under higher level phenomena such as biogeographic patterning. Second, we have sought to integrate analyses of mechanisms with accounts of how vii viii PREFACE these mechanisms came to be through evolutionary change in the genetic repertoire of organisms. We provide examples of how mutations finely tune gene products for dealing with particular environmental challenges, and we show how entirely new biochemical potentials arise through the development of new classes of genes. Mechanism and process thus serve as integrating themes in the chapters to follow. We hope that our focus on integrative approaches to the study of biochemical adaptation will provide for readers a mode of analysis that will become a routine way of viewing many biological issues. The success of this volume will be measured in part by the degree to which we have summarized important facts and concepts—‘‘trees’’ and ‘‘forests’’—as they were known near the beginning of the 21st century, and more importantly, by whether we have taught our readers what we view to be the most effective ways of addressing questions about the mechanisms and processes of biochemical adaptation. The coming decades in this so-called ‘‘Century of Biology’’ will offer enormous opportunities and challenges. New technological approaches (such as those used for obtaining detailed informa- tion in genomics, proteomics, magnetic resonance and other imaging modalities, and remote-sen- sing field physiology, to mention a few topical areas) will vastly increase the amount of information we have before us. And, paired with new means for acquiring information, we can expect equally rapid growth in the suite of algorithms used to analyze the torrent of new data. Students of biochemical adaptation must be prepared for these advances and be ready to exploit them, at least when these new advances are relevant for our purposes. If recent history is an indication of what the following decades will bring, progress in biochemical adaptation will often depend on successful incorporation of methods and theories developed for ‘‘model’’ organisms like humans, fruit flies, or zebra fish into investigations of organisms of interest to the comparative biologist. However, novel technologies per se do not necessarily and inevitably lead to creativity and advancement of a field. Comparative biologists interested in biochemical adaptation must not lose sight of the important questions and principles of their field, even as they incorporate new theories and methods from sister disciplines in biology. To the degree that we are able to adapt new approaches when applicable to long-standing questions about adaptation, our field will enjoy an even brighter future. We hope that this volume serves in some small way as a stimulus to these endeavors. Completing this volume would not have been possible without the support of many of our colleagues. First and perhaps foremost, PWH wishes to thank a group of graduate and postdoc- toral research students: Chris Moyes, Les Buck, Chris Doll, Tim West, Steve Land, Jim Staples, Mark Mossey, Petra Motishaw, Mark Trump, Gary Burness, Grant McClelland, Sheila Thornton, Gunna Weingartner, Jim Rupert, Charles Darveau, Cheryl Beatty, Peter Arthur, Kevin Campbell, and Yan Burrelle. Many of PWH’s insights are really products of their creativity, enthusiasm, and hard labor. Additionally, several colleagues have been hugely instrumental in ‘‘pulling reptilian scales’’ off of PWH’s eyeballs so that he could ‘‘see’’ better. Space will not permit mentioning all of these, but will allow especial thanks to Raul Suarez, Michael Guppy, Gordon Matheson, Carlos Monge, Peter Allen, Bob Boutilier, Dave Jones, Bill Driedzic, Dan Costa, Barbara Block, Brian Murphy, Michael Hogan, Peter Lutz, and Keith Webster. Each in their own way made PWH aware of aspects of adaptation that he otherwise would have overlooked or under emphasized. Warren Zapol, an ever-fussing deeply committed friend and colleague, has been aware (and, along with Mont Liggins, has kept PWH as aware as possible) of clinical implications of many aspects of adaptational biochemistry. Dick Taylor (until his premature death) and Ewald Weibel were con- tinuous sources of inspiration and their questions at physiological levels of organization often created intellectual fun and fermentation for those of us working at molecular and metabolic levels of organization. GNS, too, wishes to thank his current and former students and postdoctoral associates, all of whom have provided inspiration and encouragement, not to mention loads of interesting data, many of which will be found in this volume. Several of these colleagues have been generous with PREFACE ix their time and energy in helping develop the ideas and exposition of the present volume. In particular, gratitude is owed to Dr. Peter Fields, who did yeoman service as a critic and editor throughout the writing of chapters 1, 6 and 7, and Drs. Glenn Johns, Dietmar Ku¨ ltz, Jason Podrabsky, Jonathon Stillman, and Lars Tomanek, who played important roles in critiquing chapters 6 and 7. Development of many of the ideas found in the book benefited from discussions with Drs. Barb Block, D. Wayne Bolen, John Carpenter, Jim Childress, Mary Clark, Andy Cossins, Elizabeth Dahlhoff, Mark Denny, Dave Epel, Allen Gibbs, Andy Gracey, Steve Hand, Gretchen Hofmann, Linda Holland, Jen-Jen Lin, Philip Low, Donal Manahan, Eric Sanford, Serge Timasheff, Patrick Walsh, Paul Yancey, and Tzung-Horng Yang, and with current doctoral students, Rachael Ream and Caren Braby. Students in Stanford University’s course in Ecological and Evolutionary Physiology also played important editorial roles, through critiquing handouts that were based on embryonic versions of book chapters. One of the special joys of our profession sometimes arises from following the experimental organism under study to its natural habitat; or, as Per Scholander would have put it, great joy arises from taking the laboratory to the study organism rather than vice versa. In this context, we both would like to acknowledge our numerous colleagues around the world who have made, and in most cases continue to make, the entire endeavor more interesting by combining the adventures of intellect with the adventures of scientific expedition. In addition, we wish to express our deepest sense of gratitude to Brenda and Amy, who have accepted with comforting humor that Peter and George (respectively) are fundamentally ‘‘worka- holic’’ husbands, who year after year are almost certain to find excuses for shorter-than-planned holidays so that they can pursue varied academic projects. Claire, Gail, Gareth, and (until lately) Panda supplied comic relief, encouragement and support to PWH even at the lowest moments in life—when his cranial nerves were trashed by a nasty virus and death was at his door. GNS’ spirits enjoyed continual buoyancy from Gabe, whom he thanks along with Patty and Bud, who made Gabe’s entry into the family possible. GNS would not have been able to complete his part of the bargain without substantial support from the faculty and staff at the Hopkins Marine Station; they established a working environment in which it was possible to juggle teaching, research, and administrative duties while retaining sufficient ATP to complete this volume. Lastly, we thank Ms. Diana McPhail, Mr. Chris Patton and Ms. Freya Sommer for their work on illustrations, and our editor, Kirk Jensen, for unrivalled if unrequited patience. Ms. Lissa Herschleb designed for us a cover creature that aptly portrays, at an anatomical level, the concept of ‘‘unity in diversity,’’ which serves as a unifying theme in our treatment of biochemical adapta- tion. The smile on the imaginary creature’s face may be taken as a reflection of the pleasure we have had in reviewing the fascinating topics that constitute the literature of our field. We hope that the book brings our readers a comparable sense of enjoyment. Peter W. Hochachka Vancouver, British Colombia George N. Somero Pacific Grove, California