At the Board of Directors meeting held at the Hokkaido University Tokyo Office on June 2, 2018, candidates for each award were recommended to the Board of Directors following a rigorous screening by the Selection Committee for Awards. As a result of deliberations by the Zoological Society of Japan Board of Directors, it was decided to confer the 2018 Zoological Society of Japan Awards as follows.
Zoological Society of Japan
FY2018 Zoological Society of Japan Award for Encouragement: 3 recipients
Shiba Kogiku
Assistant Professor, Shimoda Marine Research Center, University of Tsukuba
Research on elucidating the mechanism of high-speed flagellar and ciliary motility through the development of visualization and imaging technologies
Reason for the award
Member Xiaoju Chai independently developed an optical microscope analysis device incorporating a high-intensity LED strobe illumination system and software, with the objective of elucidating the regulatory mechanism of flagellar and ciliary motility in rapidly moving eukaryotes. Furthermore, using the developed device, she succeeded for the first time in the world in imaging calcium dynamics when sperm change their direction of movement in response to sperm attractants, based on the fluorescence image of an indicator incorporated into the sperm. This technology can be applied not only to the analysis of flagellar and ciliary motility, but also to motility analysis systems in various bioscience-related fields, leading to numerous collaborative research projects both domestically and internationally. Highly evaluated internationally and expected to play an active role as a researcher leading future zoology, it was decided to present the Zoological Society of Japan Encouraging Award to Member Chai.
Winner Summary
Eukaryotic flagella and cilia are important motor organs for sperm motility, plankton swimming, and body fluid regulation, and their structures and functions are highly conserved through evolution. In the human body as well, flagella and cilia exist everywhere, including the brain, trachea, kidneys, sensory organs, and sperm, and it is known that the deletion of flagellar and cilia-constituting factors causes serious diseases such as hydrocephalus, bronchitis, and infertility. In my graduation research, seeing the smooth waveform changes produced by sea urchin larval cilia, and learning that this movement originates from a highly precise and beautiful structure called the 9+2 structure, which consists of microtubules and the motor protein dynein, sparked my interest in the movement control mechanisms of flagella and cilia. Furthermore, using marine organisms as my main experimental materials, I have worked on the development and application of visualization and imaging technologies to perform functional analysis of flagella and cilia, which exhibit minute and high-speed movements.
From my undergraduate graduation research through my doctoral program under the supervision of Professor Shoji Baba at Ochanomizu University, I acquired the skills to develop a microscope illumination system using an LED as a strobe light and to analyze massive waveform image data using Bohboh, a cell motility analysis software programmed by Professor Baba. Based on this, I conducted research on the regulatory mechanisms of sperm flagellar motility in sea urchins and starfish by egg-derived sperm-activating substances.1,2After obtaining my degree, armed with the techniques I had acquired, I worked on the research of ascidian sperm chemotaxis control at the Misaki Marine Biological Station of the University of Tokyo. Using visualization technology for intracellular calcium concentration within the sperm flagellum during high-speed movement, I discovered that the flagellar waveform changes required for directional changes as sperm approach the egg are triggered by a rapid increase in intracellular calcium within the flagellum.3Since 2009, at the Shimoda Marine Research Center of the University of Tsukuba, [research has shown] that the ascidian sperm protein calaxin directly regulates dynein via calcium signals and is involved in sperm chemotaxis.4Role of adenylyl cyclase in ascidian sperm motility5sperm retrograde movement mechanism in internal fertilization snails6clarified etc. Furthermore, in collaborative research responsible for flagellar motility analysis and intracellular imaging, we visualized calcium signals directly involved in sea squirt sperm self-incompatibility7, squid sperm self-assembly and CO2Discovery of chemotaxis8Discovery of sperm calcineurin, which is essential for normal motor control and fertility9contributed to.
Flagella and cilia undergo high-speed movement while responding to the surrounding environment to instantaneously regulate their motion, playing a role not only in sperm chemotaxis but also in various biological reactions. By making full use of the unique flagellar and ciliary movement visualization and imaging technologies that I have cultivated thus far, I would like to continue elucidating the mechanisms of flagellar and ciliary movement control common to eukaryotes.
Since my student days, I have conducted research using marine organisms, and at various marine biological stations both in Japan and abroad, I have had invaluable experiences such as collecting specimens, interacting with researchers, and encountering a diverse array of life. Finally, I would like to express my gratitude to everyone I have met through the marine biological stations and collaborative research.
References: 1. Shiba et al.Zoological Science(2005), 2. Shiba et al.Zygote(2006), 3. Shibaet al.PNAS(2008), 4. Mizunoet al.PNAS(2008), 5. Shibaet al.Int J Mol Sci(2014), 6. Shibaet al.J Exp Biol(2014), 7. Saitoet al.PNAS(2008), 8. Hirohashiet al.Curr Biol (2008), 9. Miyataet al.Science (2015)
Takeuchi Yuichi
Assistant Professor, Department of Medicine (Graduate School of Medicine and Pharmaceutical Sciences), University of Toyama
Ecological roles and neural basis of laterality in fish
Reason for the award
For example, in humans, many people are right-handed, and language processing is localized in the left hemisphere of the cerebrum. This phenomenon is called lateralization. In recent years, it has become clear that this is not limited to humans, but is widely present in many animals as well, ranging from insects and fish to birds. To properly use the right and left sides of the body, having an asymmetrical body is not enough; an asymmetrical brain is also necessary. Both the brain and the body must be lateralized, but the underlying mechanism remains completely unknown. Member Yuichi Takeuchi has tackled this unsolved problem in behavioral science by focusing on fish, specifically freshwater cichlids inhabiting Lake Tanganyika. A species of cichlid known as a scale-eater has individuals with mouths curved either to the right or to the left. Depending on this, they attack large fish from either the left or the right side to eat scales, and these two traits have frequency-dependent fitness, keeping their populations roughly in balance. To elucidate the mechanism of this lateralization, Member Takeuchi has promoted research that transcends the boundaries of ecology, morphology, physiology, and behavior, accumulating many important findings and earning high acclaim. In anticipation of his future development, we have decided to present the Zoological Society of Japan Encouragement Award to Member Takeuchi.
Winner Summary
To understand the fundamental principles and mechanisms of animal behavior, I have systematically conducted research ranging from the nervous system to behavior and evolution, focusing on fish, insects, and crustaceans. Here, I summarize my achievements regarding "left-right asymmetry in fish," a topic I have consistently researched from my doctoral program to the present.
Scale-eating cichlid fishes inhabiting Lake Tanganyika in Africa, famous like the Galapagos Islands as a laboratory of evolutionPerissodus microlepis(Scale-eating fish) have mouths that are twisted to the right or left, and they press their mouths against the flank of prey fish to eat their scales. Field studies have shown that "left-handed" individuals, whose left body side is more developed, target the left side of their prey, while "right-handed" individuals target the scales on the right side. Subsequently, it became clear that the laterality discovered in scale-eating fish is a trait widely observed in other fish as well (Hori et al. 2017, winner of the Zoological Science Awards 2018). Furthermore, because scale-eating and piscivorous fish prey more heavily on prey with the opposite handedness to their own, laterality is thought to be deeply linked to predator-prey relationships rather than being merely a morphological left-right asymmetry. Therefore, traveling to Lake Tanganyika and focusing on shrimp-eating fish and their prey, freshwater shrimp, with the aim of elucidating the impact of laterality on predator-prey relationships, it was revealed that: [1] shrimp-eating fish exhibit asymmetry in their mouth morphology and a directional bias in their predatory behavior; [2] freshwater shrimp also exhibit a directional bias in their escape behavior; and [3] the ratios of laterality in both the shrimp-eating fish and the shrimp oscillate in synchronization with a cycle of approximately three years, and this change is driven by the effect that the minority handedness of shrimp-eating fish can prey on more shrimp (Takeuchi & Hori 2008, etc.). From the above, it was elucidated that laterality is a general phenomenon found in various aquatic animals, and that handedness in predation and escape behavior is advantageous for survival, thereby influencing population dynamics.
This type of behavioral lateralization (right- or left-handedness) is observed in many animals, including humans, and is considered an essential characteristic for fulfilling sophisticated ecological functions. However, due to the structural and functional complexity of the cranial nervous system that produces it, it remained unclear where and what kind of lateralization existed within the neural circuits. Therefore, we started from scratch to develop unprecedented breeding technology for scale-eating fish worldwide, enabling experimental analysis of scale-eating behavior. I have previously experimentally demonstrated that: [1] predatory behavior consists of five behavioral components, and there is a clear lateral bias in the body-bending movement when stripping scales; [2] this bending movement closely resembles the escape-bending movement driven by a pair of Mauthner cells located in the hindbrain (Takeuchi et al. 2012); [5] the lateralization of predatory behavior is ambiguous during the juvenile stage and becomes biased toward one side with the development of left-right asymmetry in the lower jaw, and individuals with greater asymmetry in mouth morphology ingest more scales (Takeuchi et al. 2016); and [6] the reinforcement of predatory behavior lateralization occurs through learning via scale-eating experience (Takeuchi & Oda 2017). Furthermore, I succeeded for the first time in the world in breeding scale-eating fish in captivity, and [7] initiated research on the molecular and genetic basis of lateralization, identifying a group of genes exhibiting expression specific to the right/left brain of scale-eating fish, and revealed that these are common regardless of right- or left-handedness (Takeuchi et al. 2018). Thus, scale-eating fish are ideal animals for an integrated understanding of the neural control mechanisms of lateralization. Moving forward, it is expected to advance the elucidation of the "mechanism of handedness," which has been a long-standing mystery, while also making a major contribution to understanding the construction principles of brain lateralization and the operational principles of right- and left-handed actions.
While current biological science is dominated by molecular biological research using "model animals," I hope you will appreciate that multifaceted research strategies using "non-model animals" with phenotypes suited to the theme, such as the scale-eating fish system, lead to a deeper understanding of biological phenomena.
Hitoshi Miyakawa
Associate Professor, Bioscience Education and Research Center, Utsunomiya University
Elucidation of the endocrine mechanisms controlling phenotypic plasticity in Daphnia
Reason for the award
Member Kazushi Miyakawa has energetically conducted research on the roles of endocrine mechanisms in the developmental control and induction of phenotypic plasticity in daphniids, as well as the evolution of juvenile hormone signaling in arthropods. He has clarified that juvenile hormones and ionotropic glutamate receptors are involved in induced defenses occurring as protection against natural enemies. In addition, he isolated the juvenile hormone receptor of daphniids for the first time and demonstrated that masculinization is induced by juvenile hormone signaling in the environmentally dependent sex determination, where reproduction shifts from parthenogenesis to sexual reproduction in response to environmental changes. Furthermore, he discovered that a single amino acid mutation in the juvenile hormone receptor alters ligand specificity, and his achievements showing that the diversification of juvenile hormone receptors and their downstream signals is crucial for the evolution of juvenile hormone signaling in arthropods have been highly acclaimed. Because his research on the molecular mechanisms of phenotypic plasticity in daphniids, centered on juvenile hormones, has contributed to the advancement of invertebrate endocrinology and holds great promise for future development, it has been decided to present the Zoological Science Award to Member Miyakawa.
Winner Summary
Phenotypic plasticity, the ability to alter phenotypes in response to various environmental signals, is a crucial mechanism for organisms to adapt to their environments, and understanding its regulatory mechanisms is one of the major topics in recent developmental and evolutionary biology. Using crustaceans, specifically water fleas (Daphnia), I have been conducting research to elucidate the roles of endocrine mechanisms in the developmental control and evolution of phenotypic plasticity. Daphnia exhibit numerous striking examples of phenotypic plasticity, such as "inducible defenses" where they transform into defensive morphs in the presence of predators, as well as "environmentally dependent sex determination" and "reproductive strategy shifts," where they typically reproduce clonally but produce males and switch to sexual reproduction in response to environmental changes.
Since my doctoral program, the research topic I have pursued energetically is the elucidation of the regulatory mechanisms of inducible defense in Daphnia. Although inducible defense is an extremely important phenomenon for understanding the evolutionary process of predator-prey relationships, its molecular mechanisms have remained largely unclear. By making full use of molecular and physiological methodologies, I revealed that juvenile hormone (JH) and ionotropic glutamate receptors are involved in the regulation of inducible defense, and constructed a molecular signal cascade model for its regulation.
The aforementioned JH is a hormone that plays a central role in controlling molting, metamorphosis, and reproduction across arthropods in general. It has also long been known as a substance that disrupts sex determination and induces male production when exposed to water fleas (Daphnia). After obtaining my degree and moving to the National Institute for Basic Biology, I focused on the idea that while the single hormone JH shares common functions across many arthropods, it is also involved in the control of unique phenotypic plasticity—namely, induced defense and environmentally dependent sex determination—in Daphnia. Therefore, I hypothesized that the functional differentiation of JH might be the key to arthropod evolution, and I planned a detailed comparative analysis of hormone signaling pathways between crustaceans (Daphnia) and insects. I successfully isolated the JH receptor for the first time in crustaceans from two Daphnia species, and newly established a reporter assay system using cultured mammalian cells to analyze the interaction between the hormone ligand and the receptor. As a result of analyzing the function of the juvenile hormone receptor in Daphnia using these experimental systems, it was strongly suggested that male production in Daphnia is triggered by signals mediated through the JH receptor, thereby partially elucidating the mechanism of action of endocrine-disrupting chemicals in Daphnia. Furthermore, I clarified that a single amino acid mutation occurring between the insect and Daphnia receptors strongly influences the hormone ligand specificity of each species. Because changes in ligand specificity allow for the rapid incorporation of new upstream signaling pathways, these results suggest a high evolutionary potential for the JH pathway.
Even after moving to my current affiliation, Utsunomiya University, I have continued my research on the evolution of the juvenile hormone (JH) pathway in arthropods. In recent years, as a potential factor in the diversification of JH downstream signaling, I discovered that changes have occurred between water fleas and insects in the regulatory regions of downstream factors to which the receptor, upon receiving JH, binds when functioning as a transcription factor.
All of the above achievements were made possible with the immense support of the mentors who have guided me and my colleagues. Moving forward, I aim to actively interact with researchers in various fields to explore the role that endocrine mechanisms have played in the processes by which organisms create and maintain complex biological systems, such as phenotypic plasticity.
