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The Dark Side of the Hive The Dark Side of the Hive THE EVOLUTION OF THE IMPERFECT HONEY BEE Robin Moritz and Robin Crewe 1 1 Oxford University Press is a department of the University of Oxford. It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide. Oxford is a registered trade mark of Oxford University Press in the UK and certain other countries. Published in the United States of America by Oxford University Press 198 Madison Avenue, New York, NY 10016, United States of America. © Oxford University Press 2018 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, without the prior permission in writing of Oxford University Press, or as expressly permitted by law, by license, or under terms agreed with the appropriate reproduction rights organization. Inquiries concerning reproduction outside the scope of the above should be sent to the Rights Department, Oxford University Press, at the address above. You must not circulate this work in any other form and you must impose this same condition on any acquirer. Library of Congress Cataloging- in- Publication Data Names: Moritz, Robin F. A., and Crewe, Robin M.; authors. Title: The dark side of the hive / Robin Moritz and Robin Crewe. Description: New York, NY : Oxford University Press, 2018. | Includes bibliographical references and index. Identifiers: LCCN 2018010888 | ISBN 9780190872281 Subjects: LCSH: Honeybee—Life cycles. Classification: LCC QL568.A6 M594 2018 | DDC 595.79/9156—dc23 LC record available at https://lccn.loc.gov/2018010888 1 3 5 7 9 8 6 4 2 Printed by Sheridan Books, Inc., United States of America { CONTENTS } Preface  vii Acknowledgments  ix List of Image Credits  xi 1. Introduction  1 2. Out of the Dark  7 3. A Difficult Diet  19 4. The Chemistry of Social Regulation  29 5. The Reproductive Machine  37 6. The Worker Bee in a Variety of Guises  53 7. Diseases, Pests, and Parasites  83 8. The Idiosyncrasies of Sex and Reproduction  97 9. Apiculture and Long- Suffering Bees  121 10. Dark Sides of Honey Bee Science  145 11. A Silver Lining for the Future of Bees?  153 References  159 Index  179 { PREFACE } Producing a monograph on the life history of the honey bee, Apis mellifera, may seem somewhat quixotic at first sight in view of the fact that there are a series of excellent monographs on this topic that have been published during the past three decades. However, we believe that these volumes have a bias that is too strongly focused on the harmony and the perfection of cooperation in the colony. Tom Seeley’s excellent treatises Honeybee Ecology (1985), The Wisdom of the Hive (1995), and, most recently, Honeybee Democracy (2010) have had a major influence on students of honey bee biology. Indeed, they stand out as seminal works in organismal biology in the mold of the work of von Frisch, who won the Nobel Prize for his work on honey bees. Mark Winston’s book, The Biology of the Honey Bee (1987), as well as Robin Moritz and Edward E. Southwick’s Bees as Superorganisms— An Evolutionary Reality (1991) have dealt in great detail with the marvels of cooperation inside the colony. Yet as with any complex social system, honey bee societies are prone to error, rob- bery, cheating, and social parasitism. The honey bee colony is thus far from being a harmonious, cooperative whole. It is full of individual mistakes, ob- vious maladaptations, and evolutionary dead ends. Conflict, cheating, worker inefficiency, and curious reproduction strategies all occur. The perfection that is perceived to exist in their social organization is a function of a particular exper- imental focus on the colony as a whole rather than exploring the idiosyncrasies of its individual members. The fact that honey bee colonies get by remarkably well despite many seem- ingly odd biological features that are often dismissed as aberrations requires us to focus attention on these very “aberrations” because they are central to un- derstanding all aspects of social organization. Since we have worked together for more than two decades on the chemical ecology, genetics, and evolution of parasitic honey bee workers, we believed it is now overdue to report on the plas- ticity of social organization in the honey bee colony with a view to achieving a more nuanced understand of the evolution of sociality in these insects. What we cover in this volume is not designed to suggest that the work of our colleagues and our own previous work require revision or reconsideration but, rather, provides a richer understanding of the real life of a honey bee in the colony. Our work thus focuses on the role of the individual within the colony rather than studying the colony as a biological entity (superorganism). We try to dissect the various careers a male and a female honey bee can have and their roles in colony organization. viii Preface Colonies of honey bees are made up of a number of families because the queens are multiply mated by a number of drones (males). In order to under- stand the effects of this genetic diversity within the colony, we provide a thor- ough discussion of how the variance of individual worker phenotypes drives self- organized processes in a colony. In addition, we show how competition using both physical force and chem- ical signaling drives colonial organization. Here, we deal with handicaps that limit the use of physical force and the chemical arms races that drive competi- tion in relation to worker reproduction. This monograph focuses on bees as individuals in the colony. The story that we tell spans the full range of biological disciplines ranging from genomics to systems biology. We explore the situations in which individual interests are pursued often at the expense of the colony, and we show that the solutions that have evolved are often less than optimal. { ACKNOWLEDGMENTS } This volume would not have been possible without Anne and Mary allowing us to drone on endlessly about honey bees when indeed we should have been much more polite and addressed other more important topics. We are deeply indebted for this indulgence and have no really convincing ideas about how to repay it, particularly because we are not certain that this may not happen again despite solemn undertakings. We are also grateful to the late Ingemar Fries, Christian Pirk, Anja Buttstedt, and two anonymous reviewers for providing many important comments that markedly improved the text. We considered most of those, but not all; therefore, any errors and misconceptions remain ours and cannot be blamed on others. The generous funding of many different public institutions and funding or- ganizations that in turn received their money from the taxpayers in Germany, South Africa, and also all European Union member states allowed us to study honey bee biology over several decades. It was this long period of familiarity with honey bee biology that made us bold enough to face the challenge of writing this volume. During the actual writing phase, this project was significantly facilitated by the receipt of the Harry Oppenheimer Fellowship Award from the Oppenheimer Memorial Trust that allowed RMC to take periods of extended leave in Germany each year from 2014 to 2017. This leave allowed us to work together on the preparation of the manuscript and also to encourage doctoral students to pursue new lines of research.

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