Advances in Parasitology, Volume 70: Parasitoids of Drosophila
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Advances in PARASITOLOGY VOLUME 70 Parasitoids of Drosophila SERIES EDITORS D. ROLLINSON Department of Zoology The Natural History Museum London, UK S. I. HAY Spatial Epidemiology and Ecology Group Tinbergen Building Department of Zoology University of Oxford South Parks Road Oxford OX1 3PS, UK EDITORIAL BOARD M. COLUZZI Department of Public Health Sciences, Section of Parasitology ‘Ettore Biocca’ ‘Sapienza – Universita` di Roma’, 00185 Roma, Italy C. COMBES Laboratoire de Biologie Animale, Universite´ de Perpignan, Centre de Biologie et d’Ecologie Tropicale et Me´diterrane´enne, 66860 Perpignan Cedex, France D. D. DESPOMMIER Division of Tropical Medicine and Environmental Sciences, Department of Microbiology, Columbia University, New York, NY 10032, USA J. J. SHAW Instituto de Cieˆncias Biome´dicas, Universidade de Sa˜o Paulo, 05508-990, Cidade Universita´ria, Sa˜o Paulo, SP, Brazil K. TANABE Laboratory of Malariology, International Research Center of Infectious Diseases, Research Institute for Microbial Diseases, Osaka University, Suita 565-0871, Japan Advances in PARASITOLOGY VOLUME 70 Parasitoids of Drosophila Edited by GENEVIE`VE PRE´VOST Laboratoire de Biologie des Entomophages Universite´ de Picardie–Jules Verne Amiens cedex, France AMSTERDAM • BOSTON • HEIDELBERG • LONDON NEW YORK • OXFORD • PARIS • SAN DIEGO SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO Academic Press is an imprint of Elsevier Academic Press is an imprint of Elsevier 32 Jamestown Road, London, NW1 7BY, UK 525 B Street, Suite 1900, San Diego, CA 92101-4495, USA 30 Corporate Drive, Suite 400, Burlington, MA 01803, USA Radarweg 29, PO Box 211, 1000 AE Amsterdam, The Netherlands First edition 2009 Copyright # 2009 Elsevier Ltd. 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, mechani- cal, photocopying, recording or otherwise without the prior written permission of the publisher. Permissions may be sought directly fromElsevier’sScience&Technology Rights Department in Oxford, UK: phone (þ44) (0) 1865 843830; fax (þ44) (0) 1865 853333; email: [email protected]. Alternatively you can submit your request online by visiting the Elsevier web site at http:// elsevier.com/locate/permissions, and selecting Obtaining permission to use Elsevier material. Notice No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made. ISBN: 978-0-12-374792-1 ISSN: 0065-308X For information on all Academic Press publications visit our website at www.elsevierdirect.com Printed and bound in UK 0910111210987654321 CONTENTS Contributors xi Preface xv Introduction xvii SECTION I. ECOLOGY OF DROSOPHILA PARASITOIDS 1 1. Ecology and Life History Evolution of Frugivorous Drosophila Parasitoids 3 Fre´de´ric Fleury, Patricia Gibert, Nicolas Ris, and Roland Allemand 1.1. Distribution, Community Structure and Ecological Interactions 6 1.2. Drosophila Parasitoid Life Histories 15 1.3. Geographical Differentiation and Local Adaptation 28 1.4. Concluding Remarks 33 References 35 2. Decision-Making Dynamics in Parasitoids of Drosophila 45 Andra Thiel and Thomas S. Hoffmeister 2.1. Introduction 46 2.2. Levels of Plasticity 46 2.3. Relative Value of Hosts and Patches 48 2.4. Host Patch Detection 50 2.5. Prepatch Experience and (Initial) Leaving Tendency 51 2.6. The Effects of Intrapatch Experience 54 2.7. The Patch-Leaving Decision 56 2.8. Genetic Differences in Searching Behavior 57 2.9. Predation and Starvation 59 2.10. Prospects and Implications 60 Acknowledgments 61 References 61 3. Dynamic Use of Fruit Odours to Locate Host Larvae: Individual Learning, Physiological State and Genetic Variability as Adaptive Mechanisms 67 Laure Kaiser, Aude Couty, and Raquel Perez-Maluf 3.1. Introduction 68 3.2. General Material and Methods 71 v vi Contents 3.3. Dynamics of Odour Memory Displayed in Odour Choices 73 3.4. Dynamics of Odour Memory Displayed in Probing Behavior 77 3.5. Motivation Influences the Learned Searching Responses 81 3.6. Genetic Variability of the Learned Searching Response 83 3.7. Probing in Response to Fruit Odour: When is it Adaptive? 84 3.8. General Discussion and Conclusions 89 Acknowledgements 91 References 91 SECTION II. THE PHYSIOLOGY AND GENETICS OF IMMUNITY RELATIONSHIPS BETWEEN PARASITOIDS AND THEIR DROSOPHILA HOSTS 97 4. The Role of Melanization and Cytotoxic By-Products in the Cellular Immune Responses of Drosophila Against Parasitic Wasps 99 A. Nappi, M. Poirie´, and Y. Carton 4.1. Introduction 100 4.2. Hemocyte-Mediated Encapsulation 103 4.3. Melanization During the Drosophila Cellular Immune Reaction 103 4.4. Cytotoxic Molecules Associated with Melanization 107 4.5. The Prevention of Phenoloxidase Activity by Parasitoid Virulence Factors 113 4.6. Conclusions 115 References 116 5. Virulence Factors and Strategies of Leptopilina spp.: Selective Responses in Drosophila Hosts 123 Mark J. Lee, Marta E. Kalamarz, Indira Paddibhatla, Chiyedza Small, Roma Rajwani, and Shubha Govind 5.1. Introduction 124 5.2. The Host Range of L. boulardi and L. heterotoma 126 5.3. Origin of L. heterotoma/L. victoriae VLPs and their Effects on Host Hemocytes 134 5.4. Host Gene Expression Changes After L. boulardi and L. heterotoma Infection 138 5.5. Concluding Remarks 141 Acknowledgments 142 References 143 Contents vii 6. Variation of Leptopilina boulardi Success in Drosophila Hosts: What is Inside the Black Box? 147 A. Dubuffet, D. Colinet, C. Anselme, S. Dupas, Y. Carton, and M. Poirie´ 6.1. Introduction 148 6.2. Dissection of the Natural Variation of Encapsulation 149 6.3. Host Resistance: Origin of Variation 158 6.4. Parasitoid Virulence: Origin of Variation 163 6.5. Discussion 174 Acknowledgments 183 References 183 7. Immune Resistance of Drosophila Hosts Against Asobara Parasitoids: Cellular Aspects 189 Patrice Eslin, Genevie`ve Pre´vost, Se´bastien Havard, and Ge´raldine Doury 7.1. Introduction 190 7.2. The Immune System in D. melanogaster 191 7.3. Encapsulation: A Story Based on Quantities 195 7.4. But Does Quality Matter? The Case of the Obscura Group 207 7.5. Discussion and Concluding Remarks 208 Acknowledgment 212 References 212 8. Components of Asobara Venoms and their Effects on Hosts 217 Se´bastien J.M. Moreau, Sophie Vinchon, Anas Cherqui, and Genevie`ve Pre´vost 8.1. Introduction 218 8.2. Anatomy of the Venom Apparatus within the Asobara Genus 219 8.3. The Venom of A. tabida 224 8.4. The Venom of A. japonica 227 8.5. Expected Prospects from Studying Venoms in the Asobara Genus 228 Acknowledgments 230 References 230 viii Contents SECTION III. STRATEGIES AND EVOLUTION OF PARASITOID VIRULENCE AND HOST RESISTANCE 233 9. Strategies of Avoidance of Host Immune Defenses in Asobara Species 235 Genevie`ve Pre´vost, Ge´raldine Doury, Alix D.N. Mabiala-Moundoungou, Anas Cherqui, and Patrice Eslin 9.1. Introduction 236 9.2. Conformer Versus Regulator Strategy 237 9.3. Arms Developed by Asobara Parasitoids to Regulate or Evade Host Immunity Defenses 246 9.4. Concluding Remarks and Prospects 250 References 251 10. Evolution of Host Resistance and Parasitoid Counter-Resistance 257 Alex R. Kraaijeveld and H. Charles J. Godfray 10.1. Introduction 258 10.2. Drosophila melanogaster and its Parasitoids 259 10.3. Geographic Variation 261 10.4. Experimental Evolution of Resistance and Counter-Resistance 264 10.5. Costs of Resistance and Counter-Resistance 268 10.6. Behavior Related to Resistance and Counter-Resistance 271 10.7. Parasitoids as Hosts 274 10.8. Genetics and Genomics 274 10.9. Concluding Remarks 276 References 277 11. Local, Geographic and Phylogenetic Scales of Coevolution in Drosophila–Parasitoid Interactions 281 S. Dupas, A. Dubuffet, Y. Carton, and M. Poirie´ 11.1. Introduction 282 11.2. The Local Coevolutionary Dynamics 284 11.3. The Components of the Geographic Mosaic of Coevolution 289 11.4. Hypothesis of Coevolutionary Diversification 291 11.5. Ancestral Traits and Phylogenetic Constraints on Coevolution 292 11.6. Conclusion 292 References 293 Contents ix SECTION IV. SYMBIOTIC ORGANISMS OF DROSOPHILA PARASITOIDS 297 12. Drosophila–Parasitoid Communities as Model Systems for Host–Wolbachia Interactions 299 Fabrice Vavre, Laurence Mouton, and Bart A. Pannebakker 12.1. Introduction 300 12.2. Pattern of Infection and Phylogenetic Diversity of Wolbachia in Drosophila Parasitoids 302 12.3. Phenotypic Diversity of Wolbachia in Drosophila Parasitoids 308 12.4. Stability, Regulation and Consequences of Multiple Wolbachia Infections 317 12.5. The Role of Wolbachia in the Interaction Between Parasitoids and Hosts 320 12.6. Conclusion 323 Acknowledgments 325 References 325 13. A Virus-Shaping Reproductive Strategy in a Drosophila Parasitoid 333 Julien Varaldi, Sabine Patot, Maxime Nardin, and Sylvain Gandon 13.1. Introduction 334 13.2. Main Effect and Transmission of LbFV 335 13.3. Adaptive Significance of Superparasitism Alteration: A Modelization Approach 337 13.4. Effect of LbFV on Other Phenotypic Traits 340 13.5. Adaptive Significance of the Phenotypic Alteration Induced (Except Superparasitism) 346 13.6. Evolution in Relation to the Frequency of Horizontal Versus Vertical Transmission 348 13.7. Experimental Evolution in Relation to Transmission