Insect Taste EXPERIMENTAL BIOLOGY REVIEWS Environmental Stress and Gene Regulation Sex Determination in Plants Plant Carbohydrate Biochemistry Programmed Cell Death in Animals and Plants Biomechanics in Animal Behaviour Cell and Molecular Biology of Wood Formation Molecular Mechanisms of Metabolic Arrest Environment and Animal Development: genes, life histories and plasticity Brain Stem Cells Endocrine Interactions of Insect Parasites and Pathogens Vertebrate Biomechanics and Evolution Osmoregulation and Drinking in Vertebrates Host–Parasite Interactions The Nuclear Envelope The Carbon Balance of Forest Biomes Comparative Genomics and Proteomics in Drug Discovery The Eukaryotic Cell Cycle Drosophila: A Toolbox for the Study of Neurodegenerative Disease Practical Systems Biology Insect Taste Edited by PHILIP L. NEWLAND School of Biological Sciences, University of Southampton, Southampton, UK MATTHEW COBB Faculty of Life Sciences, University of Manchester, Manchester, UK FRÉDÉRIC MARION-POLL INRA Centre de Versailles, Paris, France Published by: Taylor & Francis Group In US: 270 Madison Avenue New York, NY 10016 In UK: 2 Park Square, Milton Park Abingdon, OX14 4RN This edition published in the Taylor & Francis e-Library, 2009. To purchase your own copy of this or any of Taylor & Francis or Routledge’s collection of thousands of eBooks please go to www.eBookstore.tandf.co.uk. © 2009 by Taylor & Francis Group First published 2009 ISBN 9780415436397 This book contains information obtained from authentic and highly regarded sources. Reprinted material is quoted with permission, and sources are indicated. A wide variety of references are listed. Reasonable efforts have been made to publish reliable data and information, but the author and the publisher cannot assume responsibility for the validity of all materials or for the consequences of their use. All rights reserved. No part of this book may be reprinted, reproduced, transmitted, or utilised in any form by any electronic, mechanical, or other means, now known or hereafter invented, including photocopying, microfi lming, and recording, or in any information storage or retrieval system, without written permission from the publishers. A catalogue record for this book is available from the British Library. Library of Congress Cataloging-in-Publication data Insect taste / edited by Philip L. Newland, Matthew Cobb. p. cm. -- (Experimental biology reviews) Includes bibliographical references. ISBN 978-0-415-43639-7 1. Insects--Physiology. 2. Taste. I. Newland, Philip L. II. Cobb, Matthew QL495.I49857 2008 573.8’78157--dc22 2008024269 Editor: Elizabeth Owen Editorial Assistant: Sarah E. Holland Production Editor: Karin Henderson Typeset by: Saxon Graphics Ltd, Derby Printed by: Cromwell Press ISBN 0-203-86675-4 Master e-book ISBN Taylor & Francis Group is the Academic Division of T & F Informa plc Visit our web site at http://www.garlandscience.com Contents Contributors xi Preface xiii 1. Gustation in Drosophila melanogaster 1 Matthew Cobb, Kristin Scott and Michael Pankratz 1 Introduction 1 2 Gustation in Drosophila larvae 2 2.1 The ecology of larval gustation 2 2.2 The neuroanatomy of larval gustation 3 2.3 Methods and problems in measuring larval gustation 8 3 Gustation in adult Drosophila 15 3.1 The gustatory system of adult Drosophila melanogaster 15 3.2 Early studies of taste selectivity in Drosophila 15 3.3 The molecular identifi cation of sugar- and bitter-sensing cells 16 3.4 Taste cells that detect other tastes 18 3.5 Comparison of taste coding strategies in the periphery for mammals and fl ies 19 3.6 Taste representations in the Drosophila brain 19 3.7 Behavioural assays to study taste in Drosophila 20 4 Taste, feeding and mating 22 4.1 Larvae and adults: growth versus reproductive needs 23 4.2 Convergence of gustatory and pheromonal signalling 24 4.3 SOG, tritocerebrum and beyond 25 4.4 Neuromodulation of central circuits 28 5 Conclusions 29 References 30 2. Drosophila Gr5a: expression pattern, ligand profi le and transduction pathway 39 Sylwester Chyb 1 Introduction 39 2 A taste case study: Drosophila Gr5a 42 3 A research strategy 43 4 Expression pattern and axonal projections 44 5 Ligand profi le 46 6 Signal transduction 50 7 The future outlook 54 Acknowledgements 55 References 55 VI CONTENTS 3. Neurophysiology of gustatory receptor neurones in Drosophila 59 Teiichi Tanimura, Makoto Hiroi, Tsuyoshi Inoshita and Frédéric Marion-Poll 1 Introduction 59 2 Taste organs in Drosophila 60 3 Electrophysiological characterisation of labellar chemosensilla 61 3.1 Method: taste recordings in Drosophila 61 3.2 Tungsten microelectrode recording 62 3.3 Spontaneous activity from GRNs 64 3.4 Comparison of signals between tip recording and tungsten recording 64 3.5 Recordings from sugar and bitter sensing neurones 64 3.6 Summary 65 4 Differential responses among labellar taste bristles 65 4.1 Types of GRNs in Drosophila 65 4.2 Variation of response among labellar taste bristles 67 4.3 Candidate receptor genes and physiology of GRNs 68 4.4 Summary 69 5 Identifi cation of water gustatory receptor neurones 69 5.1 Water taste cell 69 5.2 Enhancer trap method 70 5.3 Central projection of gustatory receptor neurones 70 6 Conclusions 72 References 73 4. Chemosensory regulation of feeding in the blowfl y: several studies after ‘The Hungry Fly’ 77 Mamiko Ozaki and Tadashi Nakamura 1 Introduction 77 2 Sweetness for the fl y: gustatory triggers for feeding 78 2.1 Sugar receptor cell 81 2.2 Sugar receptor 82 2.3 G-proteins 83 2.4 Cyclic nucleotides, IP and Ca2+ 84 3 2.5 Synergic effects 87 3 Bitterness for the fl y: gustatory avoidance of feeding 87 4 Bitter taste receptor cell (fi fth cell) 89 4.1 Noxious or bitter substance detection system 89 4.2 Lipophilic substances and gustatory OBP 91 5 Regulation of feeding 92 5.1 Olfactory modifi cation of feeding 92 5.2 Monoamines and feeding regulation 93 5.3 Blood sugar level and feeding regulation 94 6 Conclusions 95 References 96 CONTENTS VII 5. Tasting in plant-feeding insects: from single compounds to complex natural stimuli 103 Joop J.A.van Loon, Qingbo Tang, Honglei Wang, Chenzhu Wang, Dongsheng Zhou and Hans M. Smid 1 Introduction: coding principles in gustatory systems of herbivorous insects 103 2 The sense of taste of plant-feeding insects: current status is based on studies using single compounds 104 2.1 Taste neurone typology 104 2.2 Coding concepts 105 3 Binary mixtures: non-linearity in the periphery 105 4 Input–output relationships for taste-mediated behaviour 107 4.1 Larval insects 107 4.2 Adult insects 108 5 Complex mixtures: taste neurone activity and behavioural responses to real-life plant-derived stimuli 110 5.1 Changing paradigms: moving from binary mixtures to complex plant-derived mixtures 110 5.2 Multi-neural recordings: obstacles in analysis and interpretation 110 5.3 Taste neurone identifi cation using activity-related labelling 111 5.4 Taste coding in host-plant preference 113 6 Modulation of taste neurone sensitivity: opportunities to distinguish qualitative and quantitative aspects of taste coding 118 7 Conclusions and outlook 119 References 120 6. Tasting toxicants as bitter: phytoecdysteroids 127 Frédéric Marion-Poll, Delphine Calas, Dalida Darazy-Choubaya, Cécile Faucher and Charles Descoins 1 Introduction 127 2 Phytoecdysteroids as plant defence secondary compounds 128 2.1 Phytoecdysteroids: a family of molecules 128 2.2 Botanical distribution, synthetic pathways 129 2.3 Defence compounds: tissue distribution, inducibility, turnover 129 3 Phytoecdysteroids are toxic to insects 129 3.1 Toxicity of diet ecdysteroids 129 3.2 Detoxifi cation pathways 130 3.3 Different types of insects affected 131 4 Phytoecdysteroids as toxic molecules and antifeedants to larval Lepidoptera 132 4.1 Behavioural effects 132 4.2 Taste detection 133 5 Phytoecdysteroids and adult Lepidoptera 134 5.1 Toxicity? 134 5.2 Taste detection 134 5.3 Anti-oviposition effects of ecdysteroids 134 VIII CONTENTS 6 Conclusions 135 References 135 7. Peripheral modulation of taste responses 139 Hansjürgen Schuppe and Philip L. Newland 1 Introduction 139 1.1 Locusts as model organisms for the study of taste and nutritional regulation 139 1.2 How locusts detect taste 139 1.3 Taste responses in locusts 143 1.4 The link with behaviour 144 1.5 Tracing the neural circuits 147 2 The role of chemosensory responses in nutritional regulation 149 2.1 Nutritional requirements and the need to balance the diet 149 2.2 Modulation of the phagostimulatory power at different levels 149 2.3 Mechanisms that modulate taste responses 154 3 Modulation of taste responses by NO 158 3.1 Early role for NO in chemosensory processing and feeding 158 3.2 NO in taste organs of vertebrates 161 3.3 NO and taste modulation in insects 162 4 A role for NO in the peripheral regulation of nutrient intake 169 4.1 Regulation of salt responses via peripheral NO synthesis 169 4.2 Balancing food intake via the periphery 171 References 173 8. The ‘sweet tooth’ of the honeybee: the perception of nectar and its infl uence on honeybee behaviour 183 Geraldine A. Wright 1 Introduction 183 2 Gustatory environment of honeybees 183 2.1 Nectar 183 2.2 Nectar’s nutrients 184 2.3 Other compounds 185 2.4 Variation in nectar quality 186 3 The honeybee’s sweet tooth 187 3.1 Peripheral mechanisms of gustation 187 3.2 Central organisation of honeybee taste 190 3.3 Proboscis extension refl ex (PER) 192 4 Gustatory perception and behaviour 193 4.1 Sucrose 193 4.2 Modulation of gustatory sensitivity to sucrose 194 4.3 Other compounds 196 5 Conclusions 197 Acknowledgements 198 References 198 CONTENTS IX 9. Effects of experience on the physiology of taste discrimination in insects 205 Marta L. del Campo, Carol I. Miles and Marina C. Caillaud 1 Introduction 205 1.1 Experience: a fundamental modifi er of feeding behaviour 206 1.2 Central nervous system, sensory input and feeding behaviour 207 2 Taste organs: anatomy and distribution 208 2.1 Taste neurones 210 2.2 Membrane receptors 211 2.3 Ion Channels, second messengers and intracellular cascades 212 2.4 Sensillar fl uid 214 3 The neurophysiology of taste in insects: from transduction to coding 215 3.1 Stimulants, deterrents and the reality of mixtures: selecting meaningful fl avours 219 3.2 The diversity of taste neurone responses 220 4 Experience as a modifi er of taste neurone input in insects 222 4.1 A case study: induction of host specifi city in a facultative specialist feeder, the larvae of Manduca sexta 223 4.2 Neural circuitry for feeding choices among host-restricted and polyphagous Manduca larvae 225 4.3 Molecular basis of experience-based changes of taste neurone input in Manduca larvae 227 5 Conclusions and future directions 231 Acknowledgements 231 References 232 10. Evolutionary biology of learning in insects: the search for food 243 Frédéric Mery 1 Introduction 243 1.1 What is learning? 243 1.2 Different forms of learning 244 1.3 When is learning advantageous? 245 2 Variation in learning ability in nature 246 2.1 Inter- and intraspecifi c variation in learning ability 246 2.2 Do generalists learn better than specialists? 248 2.3 Effect of environmental conditions on the development of memory 249 3 Cost and constraints of learning 250 3.1 Costs of being naive 250 3.2 Constitutive costs of learning 250 3.3 Induced costs of learning 250 3.4 Memory constraints in insect and fl ower constancy 251 4 Conclusion and perspectives 251 References 252 Index 257