The Cricket As a Model Organism Hadley Wilson Horch • Taro Mito Aleksandar Popadic´ • Hideyo Ohuchi Sumihare Noji Editors
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The Cricket as a Model Organism Hadley Wilson Horch • Taro Mito Aleksandar Popadic´ • Hideyo Ohuchi Sumihare Noji Editors The Cricket as a Model Organism Development, Regeneration, and Behavior Editors Hadley Wilson Horch Taro Mito Departments of Biology and Graduate school of Bioscience and Bioindustry Neuroscience Tokushima University Bowdoin College Tokushima, Japan Brunswick, ME, USA Aleksandar Popadic´ Hideyo Ohuchi Biological Sciences Department Department of Cytology and Histology Wayne State University Okayama University Detroit, MI, USA Okayama, Japan Dentistry and Pharmaceutical Sciences Sumihare Noji Okayama University Graduate School Graduate school of Bioscience of Medicine and Bioindustry Tokushima University Okayama, Japan Tokushima, Japan ISBN 978-4-431-56476-8 ISBN 978-4-431-56478-2 (eBook) DOI 10.1007/978-4-431-56478-2 Library of Congress Control Number: 2016960036 © Springer Japan KK 2017 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. Printed on acid-free paper This Springer imprint is published by Springer Nature The registered company is Springer Japan KK The registered company address is: Chiyoda First Bldg. East, 3-8-1 Nishi-Kanda, Chiyoda-ku, Tokyo 101-0065, Japan Preface Crickets inhabit all areas of the world with the exception of subarctic and arctic regions. Encompassing about 2,400 species, they are the most diverse lineage of the “leaping” insects. Their defining characteristic is the chirping sound made by males during mating. For the past 100 years, detailed studies at the behavioral, acoustic, and neurophysiological level have revealed fundamental aspects of mating behav- ior and the complexity of the aggressive interactions among males. Around the world, crickets are also considered an important food source. They are frequently reared on an industrial scale to satisfy demands from zoos and pet stores as well as from food processing plants. Crickets are served as a common street snack through- out Southeast Asia and can frequently be found as an ingredient in commercially produced protein bars and baked goods. Remarkably, the food conversion effi- ciency of house crickets (Acheta domesticus) is five times higher than beef, and if their fecundity is taken into account, this efficiency increases 15–20-fold (Nakagaki and Defoliart 1991). If one considers the ever-increasing human population growth, our survival on Earth may depend on altering our eating habits and consuming new sources of food, such as insects (O. Deroy 2015). The present volume aims to provide recent scientific updates on research on crickets in general, with the emphasis on Gryllus bimaculatus. We believe that this species can serve as a representative model for basal, hemimetabolous insect lineages. In this mode of development, an embryo develops into a miniature adult (first nymph), which in turn undergoes a number of successive molts before turning into an adult. In comparison, the development and overall biology of the premier insect genetic model system, Drosophila melanogaster, are highly derived and representative of only one insect group (Diptera – flies). As this book demonstrates, it is rather the cricket, as exemplified by Gryllus, which should be considered to represent a typical insect. Until recently, though, only very limited functional and genetic manipulation studies were feasible in non-drosophilid species. This all changed dramatically in the past 10 years, as the cricket community made rapid progress adapting existing and new experimental techniques in Gryllus. The main impetus behind all these advancements can be traced to the 2006 Nobel Prize in v vi Preface Physiology or Medicine to Andrew Z. Fire and Craig C. Mello for their discovery of RNA interference (RNAi). The advent of the RNAi methodology provided a powerful tool to study almost any insect species. As shown in this book, many researchers have performed functional analyses of a variety of cricket genes, yielding important information about the biology and development of this organism. In 2015, the first available rough draft assembly of the whole genome of Gryllus bimaculatus was completed at Tokushima University. This was a milestone event, enabling researchers to study hundreds of new genes (public access is planned for 2017). In addition to making transgenic crickets, it is now possible to use site-specific approaches such as TALENs and zinc-finger nucleases to alter the Gryllus genome at a targeted region. Furthermore, the CRISPR/Cas-based genome- editing system has been adapted for use in the cricket. These newly available genome-editing techniques can spearhead the detailed examination of gene func- tion and the production of gene-edited crickets that can serve as models for human diseases. In theory, such genetically engineered crickets can be used to screen various chemicals to find drug candidates for genetic disorders and to produce human therapeutic proteins or metabolites. In 2012, we organized the 2nd International Conference on Cricket Research in Tokushima, Japan. (In fact, the first conference was canceled because of the Great East Japan Earthquake of March 11, 2011.) At that second meeting, we proposed the publication of this book and invited participants to contribute chapters representing their fields and their work. We want to thank all the authors for their contributions and support throughout the development of this book. We hope that this volume will inspire scientists in various disciplines to use the cricket model system to ask interesting and innovative questions. Brunswick, ME, USA Hadley Wilson Horch Tokushima, Japan Taro Mito Tokushima, Japan Sumihare Noji Okayama, Japan Hideyo Ohuchi Detroit, MI, USA Aleksandar Popadic´ September, 2015 References Nakagaki BJ, Defoliart GR (1991) Comparison of diets for mass-rearing Acheta domesticus (Orthoptera: Gryllidae) as a novelty food, and comparison for food conversion efficiency with values reported for livestock. J Econ Entomol 84:891–896 O’Deroy O (2015) Eat insects for fun, not to help the environment. Nature 521:395 Contents Part I Development and Regeneration 1 History of Cricket Biology ............................... 3 Gerald S. Pollack and Sumihare Noji 2 Early Development and Diversity of Gryllus Appendages ........ 17 Jin Liu and Aleksandar Popadic´ 3 Leg Formation and Regeneration .......................... 31 Tetsuya Bando, Yoshimasa Hamada, and Sumihare Noji 4 Eye Development and Photoreception of a Hemimetabolous Insect, Gryllus bimaculatus ............................... 49 Hideyo Ohuchi, Tetsuya Bando, Taro Mito, and Sumihare Noji 5 An Early Embryonic Diapause Stage and Developmental Plasticity in the Band-Legged Ground Cricket Dianemobius nigrofasciatus ......................................... 63 Sakiko Shiga and Hideharu Numata Part II Physiology, Nervous System, and Behavior 6 Molecular Approach to the Circadian Clock Mechanism in the Cricket ......................................... 77 Kenji Tomioka, Outa Uryu, Yuichi Kamae, Yoshiyuki Moriyama, ASM Saifullah, and Taishi Yoshii 7 Hormonal Circadian Rhythm in the Wing-Polymorphic Cricket Gryllus firmus: Integrating Chronobiology, Endocrinology, and Evolution ............................ 91 Anthony J. Zera, Neetha Nanoth Vellichirammal, and Jennifer A. Brisson vii viii Contents 8 Plasticity in the Cricket Central Nervous System .............. 105 Hadley Wilson Horch, Alexandra Pfister, Olaf Ellers, and Amy S. Johnson 9 Learning and Memory .................................. 129 Makoto Mizunami and Yukihisa Matsumoto 10 Neurons and Networks Underlying Singing Behaviour .......... 141 Stefan Schoneich€ and Berthold Hedwig 11 The Cricket Auditory Pathway: Neural Processing of Acoustic Signals ..................................... 155 Gerald S. Pollack and Berthold Hedwig 12 Neuromodulators and the Control of Aggression in Crickets ..... 169 Paul A. Stevenson and Jan Rillich 13 Fighting Behavior: Understanding the Mechanisms of Group-Size-Dependent Aggression ....................... 197 Hitoshi Aonuma 14 Cercal System-Mediated Antipredator Behaviors .............. 211 Yoshichika Baba and Hiroto Ogawa 15 The Biochemical Basis of Life History Adaptation: Gryllus Studies Lead the Way ............................. 229 Anthony J. Zera 16 Reproductive Behavior and Physiology in the Cricket Gryllus bimaculatus ........................................... 245 Masaki Sakai, Mikihiko Kumashiro, Yukihisa Matsumoto, Masakatsu Ureshi, and Takahiro Otsubo Part III Experimental Approaches 17 Protocols for Olfactory Conditioning Experiments ............. 273 Yukihisa Matsumoto, Chihiro Sato Matsumoto, and Makoto Mizunami 18 Optical Recording Methods: How to Measure Neural Activities with Calcium Imaging ........................... 285 Hiroto Ogawa and John P. Miller 19 Trackball Systems for Analysing Cricket Phonotaxis ........... 303 Berthold Hedwig Contents ix 20 Synthetic Approaches for Observing and Measuring Cricket Behaviors ...................................... 313 Hitoshi Aonuma 21 Protocols in the Cricket ................................. 327 Hadley Horch, Jin Liu, Taro Mito, Aleksandar Popadic´, and Takahito Watanabe Index ................................................... 371.