Maki Shirae-Kurabayashi and Akira Nakamura. 2 Regulatory Mechanisms of the .... Mei Matsuzaki, Tomohiro Sasanami, Yoko Iwata, and Noritaka Hirohashi.
Diversity and Commonality in Animals Series editors Takahiro Asami Matsumoto, Japan Hiroshi Kajihara Sapporo, Japan Kazuya Kobayashi Hirosaki, Japan Osamu Koizumi Fukuoka, Japan Masaharu Motokawa Kyoto, Japan Kiyoshi Naruse Okazaki, Japan Akiko Satoh Hiroshima, Japan Kazufumi Takamune Kumamoto, Japan Hideaki Takeuchi Okayama, Japan Michiyasu Yoshikuni Fukuoka, Japan
The book series Diversity and Commonality in Animals publishes refereed volumes on all aspects of zoology, with a special focus on both common and unique features of biological systems for better understanding of animal biology. Originating from a common ancestor, animals share universal mechanisms, but during the process of evolution, a large variety of animals have acquired their unique morphologies and functions to adapt to the environment in the struggle for existence. Topics covered include taxonomy, behavior, developmental biology, endocrinology, neuroscience, and evolution. The series is an official publication of The Zoological Society of Japan. More information about this series at http://www.springer.com/series/13528
Kazuya Kobayashi • Takeshi Kitano Yasuhiro Iwao • Mariko Kondo Editors
Reproductive and Developmental Strategies The Continuity of Life
Editors Kazuya Kobayashi Department of Biology, Faculty of Agriculture and Life Science Hirosaki University Hirosaki, Japan Yasuhiro Iwao Laboratory of Reproductive Developmental Biology, Division of Earth Sciences, Biology, and Chemistry Graduate School of Sciences and Technology for Innovation Yamaguchi University Yamaguchi, Japan
Takeshi Kitano Department of Biological Sciences Graduate School of Science and Technology Kumamoto University Kumamoto, Japan Mariko Kondo Misaki Marine Biological Station Graduate School of Science The University of Tokyo Miura, Japan
ISSN 2509-5536 ISSN 2509-5544 (electronic) Diversity and Commonality in Animals ISBN 978-4-431-56607-6 ISBN 978-4-431-56609-0 (eBook) https://doi.org/10.1007/978-4-431-56609-0 Library of Congress Control Number: 2018936752 © Springer Japan KK, part of Springer Nature 2018 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. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Printed on acid-free paper This Springer imprint is published by the registered company Springer Japan KK part of Springer Nature. The registered company address is: Shiroyama Trust Tower, 4-3-1 Toranomon, Minato-ku, Tokyo 1056005, Japan
Preface
When organisms become multicellular, the specialization of cell types is established, which results in the acquisition of a variety of biological functions. During the specialization of cell types, organisms achieve the production of germ cells in which their genetic material is recombined by meiosis. To achieve effective “sex”, animals further develop male (spermatozoa) and female (eggs) germ cells. Fertilization, the fusion between a spermatozoon and an egg, requires self/non-self- recognition mechanisms and begins the process of embryogenesis. Animals accomplish genetic diversity through meiosis and fertilization. During embryogenesis, animals must produce specialized cell types in accordance with their body plan. This series of phenomena is essential to the continuity of life in the animal kingdom. This book reviews the diversity of the animal kingdom, including reproductive strategies and germ cell differentiation mechanisms, sex determination and differentiation, the mechanisms of fertilization, and body axis formation. Of particular interest is the diversity of molecules and mechanisms used to achieve the same biological purpose in different animals. This raises the question of whether or not each mechanism is conserved at a taxonomic classification level. The answer to this question will not be obvious until we examine a variety of animals: the mechanism might be the result of specialization within a certain classification level; alternatively, the mechanism identified in one animal species might be an important mechanism common to all animals. In other words, scientists may find a new common principle hidden in the diversity of molecules and mechanisms. In this book, our aim is to motivate readers to understand the universality and diversity of biological systems involved in animal reproduction and development. A brief introduction to the four parts of the book (reproductive strategies and germ cell differentiation mechanisms, sex determination and differentiation, mechanisms of fertilization, and body axis formation) is presented in the following four paragraphs. Metazoans have achieved sexual reproduction through the production of germ cells. In sexual reproduction, offspring are produced by a new combination of parental genes. This has led to an explosion of diversity in metazoans. The mechanisms leading to the differences between somatic cells and germ cells and the methods of germline stem cell (GSC) regulation are expected to be closely associated v
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with reproductive strategies. In Part I (11 chapters), the diversity associated with the mechanisms of metazoan germ cell differentiation and reproductive strategies is introduced. The separation of somatic and germ cells, referred to as the determination of primordial germ cells (PGCs), occurs via three mechanisms: preformation, epigenesis, and postembryonic germ cell development. The mechanisms associated with preformation and epigenesis have been well studied in the fly and mouse, respectively. Interestingly, in ascidians, both preformation and epigenesis occur during embryogenesis. The biological significance of these mechanisms is discussed. Gamete formation through GSC regulatory mechanisms is unique among animals. These mechanisms are well studied in the fly, medaka, and mouse. It has been reported that GSC regulation in Caenorhabditis elegans and the quail is controlled by nutritional status and seasonal changes, respectively. Some metazoans that possess pluripotent stem cells undergo postembryonic germ cell development. Typically, they reproduce asexually but develop PGCs or germ cells from pluripotent stem cells when they reproduce sexually. These organisms may switch between asexual and sexual reproduction, depending on environmental conditions and/or life cycle stage. The reproductive switching mechanisms and phenomena in hydra, jellyfish, planarians, and annelids are introduced in Part I. The reproductive switching phenomenon is also observed in the social amoeba Dictyostelium discoideum. The reproductive strategy of switching between asexual and sexual reproduction confers advantages with respect to offspring fitness. Part II (9 chapters) pertains to sex determination and differentiation in crustaceans, insects, fish, amphibians, reptiles, birds, and mammals. The sex determination system is a biological system that directs the undifferentiated embryo into a sexually dimorphic individual. Sex determination sets the stage for sex differentiation, which is established by multiple molecular events that form either a testis or an ovary. Male heterogamety (XY) is conserved in mammals and the fly; female heterogamety (ZW) is ubiquitous in birds and silkworms; and poikilothermic vertebrates (fish, amphibians, and reptiles) and crustaceans exhibit environmental sex determination systems in addition to genetic sex determination. In tropical fish, sex is completely controlled by environmental or social factors. Thus, significant diversity exists in the sex determination and differentiation mechanisms of animals. Part II summarizes the general information and recent knowledge regarding sex determination and differentiation in animals and presents current perspectives on these research fields. Sexual reproduction in animals and plants requires fertilization. Fertilization is a unidirectional chain of events leading to important changes for embryonic development, including the restoration of male and female diploid genomes and the induction of egg activation to elicit polyspermy block and to initiate cell cycles for early embryonic development. Animals have evolved a variety of elaborate molecular and cellular mechanisms to accomplish fertilization. In Part III (7 chapters), we describe the diversity of fertilization mechanisms and provide insight into the universal and key systems conserved during evolutionary processes. The following subjects are included: sperm motility and function prior to fertilization, post-copulatory reproductive strategies in sperm, sperm and egg interactions and self-sterility, and
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p olyspermy block during animal fertilization. In addition, special topics involved in the establishment of fertilization are included, such as intercellular signals for oocyte maturation, sperm–egg fusion at the plasma membrane, and protein–tyrosine kinase signaling during fertilization. When an animal is observed, what is the first thing that catches the eye? It may be the way it moves, how it behaves, the color of the body, and of course, the shape and structure of the animal. Animals can be grouped according to general body shape; among metazoans, the shapes include asymmetrical, radial, and bilateral. Asymmetry is also found in symmetrical animals. There are even animals that change their body plan during development. In Part IV (6 chapters), we focus on body axis formation and investigate how bodies are formed. To encompass this enormous diversity, we cover a broad range of taxa, from cnidarians to vertebrates, and introduce the recent understanding of body axis development. For years, biologists have been fascinated by the mechanisms for body axis development. The axes are defined by maternal and zygotic determinants at different times during development. Comparative studies have shown that there are key molecules involved in the determination of axes; furthermore, these molecules are shared among animals. This highlights the evolutionary conservation of mechanisms underlying the axis development process, a crucial concept of several chapters. Although axis determination is a conserved process, related animals do not necessarily look similar in structure. There are some unique body axes that appear to be contrary to their phylogenetic position. For example, echinoderms are classified in a sister clade to chordates and ascidians are chordates, like humans and other vertebrates; however, their body axes are significantly different. Although Part IV is not all-encompassing, we hope that readers will gain some insight into the formation of body axes and share our fascination with this process, which incorporates both conservation and diversity. This book provides new understanding of the universality of biological systems through the comparison of a variety of reproductive and developmental mechanisms. We hope that the book is useful for undergraduates, graduate students, and professional scientists who seek a greater awareness of animal reproduction and development. Hirosaki, Japan Kumamoto, Japan Yamaguchi, Japan Miura, Japan
Kazuya Kobayashi Takeshi Kitano Yasuhiro Iwao Mariko Kondo
Acknowledgments
We are very grateful to the following 46 reviewers for their insightful and constructive comments to improve the manuscripts: Ken Cho (University of California, Berkeley, USA), Charles David (Ludwig Maximilian University of Munich, Germany), Ryusaku Deguchi (Miyagi University of Education, Japan), Shogo Haraguchi (Waseda University, Japan), Nicholas D. Holland (University of California, San Diego, USA), Motonori Hoshi (Tokyo Institute of Technology, Japan), E. Jane Albert Hubbard (New York University School of Medicine, USA), Hiroshi Iida (Kyushu University Japan), Kazuo Inaba (University of Tsukuba, Japan), Hidehiko Inomata (RIKEN, Japan), Naokazu Inoue (Fukushima Medical University, Japan), Laurinda Jaffe (University of Connecticut Health Center, USA), Toshie Kai (Osaka University, Japan), Kenichi Kashimada (Tokyo Medical and Dental University, Japan), Kazuo Kawamura (Kochi University Japan), Judith Kimble (University of Wisconsin–Madison, USA), Satomi Kohno (St. Cloud State University, USA), Gaku Kumano (Tohoku University, Japan), Brian Livingston (California State University, Long Beach, USA), Michael Maxwell (National University, USA), Akira Nakamura (Kumamoto University, Japan), Hiroshi Nakato (University of Minnesota, USA), Hiroshi Namikawa (National Museum of Nature and Science, Japan), Hiroki Nishida (Osaka University, Japan), Takuya Nishigaki (Universidad Nacional Autónoma de México, Mexico), Takehiko Ogawa (Yokohama City University, Japan), Hidefumi Orii (University of Hyogo, Japan), Labib Rouhana (Wright State University, USA), Hidetoshi Saiga (Tokyo Metropolitan University, Japan), Noriyoshi Sakai (National Institute of Genetics, Japan), Mitsuru Sakaizumi (Niigata University, Japan), Tomohiro Sasanami (Shizuoka University, Japan), Yutaka Sato (Kyoto University, Japan), Takashi Shimizu (Hokkaido University, Japan), Susan Suarez (Cornell University, USA), Hiroyuki Takeda (University of Tokyo, Japan), Shin Tochinai (Hokkaido University, Japan), Toshinobu Tokumoto (Shizuoka University, Japan), Kiyotaka Toshimori (Chiba University, Japan), Hideho Uchiyama (Yokohama City University, Japan), Hideko Urushihara (University of Tsukuba, Japan), Hiroshi Wada (University of Tsukuba, Japan), Hiroshi Watanabe (Okinawa Institute of Science and Technology, Japan), Gary Wessel (Brown University, USA), Carmen Williams (National Institute of ix
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Environmental Health Sciences, USA), and Sadao Yasugi (Tokyo Metropolitan University, Japan). Moreover, we would like to express our gratitude to Prof. Kazufumi Takamune (Kumamoto University, Japan) and Prof. Motonori Hoshi (Tokyo Institute of Technology, Japan), who gave us the dedicated comments to edit this book. We also thank Dr. Misato Kochi (Springer, Japan) for her patience and kind support. Finally, we would like to profoundly thank all the authors for their expertise and hard work.
Contents
Part I Diversity in Reproductive Strategies and Germ Cell Differentiation Mechanisms 1 Germ-Cell Formation in Solitary Ascidians: Coexistence of Preformation and Epigenesis......................................... 3 Maki Shirae-Kurabayashi and Akira Nakamura 2 Regulatory Mechanisms of the Germline Stem Cell Niche in Drosophila melanogaster..................................................................... 19 Yoshiki Hayashi and Satoru Kobayashi 3 Regulation of Germline Stem Cells in the Teleost: Gametogenesis, Sex, and Fecundity....................................................... 37 Minoru Tanaka 4 Regulatory Mechanism of Spermatogenic Stem Cells in Mice: Their Dynamic and Context-Dependent Behavior............................... 47 Shosei Yoshida 5 Nutritional Control of the Germline Development in Caenorhabditis elegans........................................................................ 69 Masamitsu Fukuyama 6 Seasonal Regulation of Reproduction in Vertebrates: Special Focus on Avian Strategy............................................................. 103 Ai Shinomiya and Takashi Yoshimura 7 Roles of Germline Stem Cells and Somatic Multipotent Stem Cells in Hydra Sexual Reproduction............................................. 123 Chiemi Nishimiya-Fujisawa and Satoru Kobayashi 8 Reproductive Strategies in Marine Hydrozoan Jellyfish: Sexual Medusae and Asexual Polyps...................................................... 157 Noriyo Takeda, Ryusaku Deguchi, and Takeshi Itabashi
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9 Reproductive Strategies in Planarians: Insights Gained from the Bioassay System for Sexual Induction in Asexual Dugesia ryukyuensis Worms................................................. 175 Takanobu Maezawa, Kiyono Sekii, Masaki Ishikawa, Hikaru Okamoto, and Kazuya Kobayashi 10 Reproductive Strategies in Annelida: Germ Cell Formation and Regeneration.................................................................. 203 Ryosuke Tadokoro 11 Reproductive Strategies in Social Amoeba............................................ 223 Masashi Fukuzawa Part II Diversity in Sex Determination and Differentiation 12 Environmental Control of Sex Differentiation in Daphnia.................. 247 Kenji Toyota, Norihisa Tatarazako, and Taisen Iguchi 13 Sex Determination Cascade in Insects: A Great Treasure House of Alternative Splicing.................................................................. 267 Masataka G. Suzuki 14 Genetic Control of Sex Determination and Differentiation in Fish........................................................................................................ 289 Masaru Matsuda 15 Endocrine and Environmental Control of Sex Differentiation in Gonochoristic Fish..................................................... 307 Takeshi Kitano 16 Variety of Sex Change in Tropical Fish.................................................. 321 Yasuhisa Kobayashi, Ryo Nozu, Ryo Horiguchi, and Masaru Nakamura 17 Sex Determination and Differentiation in Frogs................................... 349 Michihiko Ito 18 Environmental Control of Sex Determination and Differentiation in Reptiles................................................................ 367 Shinichi Miyagawa, Ryohei Yatsu, and Taisen Iguchi 19 Sex Determination and Differentiation in Birds................................... 391 Asato Kuroiwa 20 Sex Determination and Differentiation in Mammals........................... 407 Kento Miura, Ayako Tomita, and Yoshiakira Kanai
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Part III Diversity in the Mechanism of Fertilization 21 Modulation of Sperm Motility and Function Prior to Fertilization................................................................................ 437 Manabu Yoshida and Kaoru Yoshida 22 Postcopulatory Reproductive Strategies in Spermatozoa.................... 463 Mei Matsuzaki, Tomohiro Sasanami, Yoko Iwata, and Noritaka Hirohashi 23 Ascidian Sexual Reproductive Strategies: Mechanisms of Sperm-Egg Interaction and Self-Sterility................... 479 Hitoshi Sawada, Shiori Nakazawa, and Maki Shirae-Kurabayashi 24 Universality and Diversity of a Fast, Electrical Block to Polyspermy During Fertilization in Animals.................................... 499 Yasuhiro Iwao and Kenta Izaki 25 Preparing for Fertilization: Intercellular Signals for Oocyte Maturation............................................................................. 535 Leia C. Shuhaibar, David J. Carroll, and Laurinda A. Jaffe 26 Regulation of Sperm-Egg Fusion at the Plasma Membrane................ 549 Kenji Miyado, Kenji Yamatoya, Woojin Kang, and Natsuko Kawano 27 Fertilization and Protein Tyrosine Kinase Signaling: Are They Merging or Emerging?........................................................... 569 Ken-ichi Sato Part IV Diversity in Axis Formation 28 Early Embryonic Axis Formation in a Simple Chordate Ascidian.................................................................................... 593 Gaku Kumano 29 Recent Advances in Hagfish Developmental Biology in a Historical Context: Implications for Understanding the Evolution of the Vertebral Elements................................................ 615 Kinya G. Ota 30 Left–Right Specification in the Embryonic and Larval Development of Amphibians............................................... 635 Ryuji Toyoizumi and Kazue Mogi 31 The Molecular Basis of the Gastrula Organizer in Amphibians and Cnidarians............................................................... 667 Yuuri Yasuoka and Masanori Taira
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32 Axis Formation and Its Evolution in Ray-Finned Fish........................ 709 Masahiko Hibi, Masaki Takeuchi, Hisashi Hashimoto, and Takashi Shimizu 33 Postembryonic Axis Formation in Planarians....................................... 743 Yoshihiko Umesono 34 Larval and Adult Body Axes in Echinoderms....................................... 763 Akihito Omori, Mani Kikuchi, and Mariko Kondo
