The Board of Directors of the Zoological Society of Japan (a public interest incorporated association) held a board meeting on Friday, June 2, 2017, and deliberated on award recipients based on the recommended candidates from the Awards Selection Committee. As a result, the recipients of the 2017 Zoological Society of Japan Awards have been decided as follows. The award ceremony, as well as the lectures by the winners of the Zoological Society of Japan Award and the Prominent Service/Encouragement Award, will be held on September 22 at the Toyama Prefectural Civic Center.
Public Interest Incorporated Foundation, Zoological Society of Japan
Chairman Yoshitaka Oka
Young Investigator Award of the Zoological Society of Japan
Moriyama Minoru
National Institute of Advanced Industrial Science and Technology, Biomedical Research Institute, Postdoctoral Researcher
Ecological, physiological, and biochemical studies on environmental adaptation in insects
Reason for winning
Member Minoru Moriyama is conducting research aimed at comprehensively elucidating the environmental adaptation strategies of insects by utilizing a diverse range of methods. In graduate school, through physiological and ecological research on the hatching strategies of cicadas, he clarified the mechanism behind the dominance of the brown cicada in urban areas. This achievement has already been featured in various media outlets. Subsequently, focusing on true bugs and weevils, he has been advancing the elucidation of nutritional adaptation mechanisms through symbiosis with microorganisms using biochemical and molecular biological approaches. By promoting research with a broad approach ranging from fieldwork to molecules and genomics, and because he is expected to play an active role as a researcher leading zoology in the future, it was decided to award the Zoological Society of Japan Encouragement Award to Member Moriyama.
Winner Summary
Insects are a highly diversified taxonomic group, and the environmental adaptation strategies that individual species have uniquely evolved in response to various environmental factors such as climate, food, and natural predators are truly diverse and exquisitely formed. For me, who wanted to actually see and touch the sophisticated environmental adaptation devices possessed by animals and unravel their mysteries through my own experimental system, insects were the ideal subject of research.
The first research topic I tackled as a student in the laboratory at Osaka City University was the environmental adaptation of cicadas. At that time, Cryptotympana facialis (Kumazemi) were already increasing, particularly in urban areas in western Japan, and the city of Osaka in particular was dominated entirely by this species. Changes in the cicada fauna, which are a traditional feature of summer, were covered by the media every year with questions like "Is this the effect of global warming?", and investigating the cause was a topic of high social interest. First, by comparing the cold tolerance of various cicada species, we clarified that C. facialis possesses sufficient cold tolerance, demonstrating that the previously hypothesized universal pathway—whereby global warming improves the overwintering survival rate of C. facialis—was not the cause. Building on this, by combining field observations, manipulative experiments, and model estimation, we proved that the temperature rise associated with urbanization accelerates the hatching timing of C. facialis, shifting it to coincide with the rainy season, which remarkably improves the hatching rate of C. facialis, a species with a mechanism of hatching in response to rain. Furthermore, we discovered that C. facialis nymphs have a remarkably superior ability to burrow into the ground compared to other cicadas, demonstrating that they predominantly inhabit urban areas where the soil is hard. As described above, we ascertained that the recent dominance of C. facialis associated with urbanization is driven by a unique mechanism of action aligned with the environmental adaptation strategies of cicadas.
After moving to the National Institute of Advanced Industrial Science and Technology (AIST), captivated by the mechanism through which insects acquire novel environmental adaptability via the functions of symbiotic microorganisms harbored within their bodies, I tackled the challenge of elucidating their molecular, biochemical, and evolutionary mechanisms. In particular, focusing on the nutritional interactions exchanged between insects and symbiotic microorganisms regarding adaptation to feeding environments, I conducted research that proved that the unique characteristics of insects—specifically, that bed bugs are hematophagous pests, bean bugs are soybean pests, and the black-backed weevil is, as its name suggests, a hard-bodied insect—are realized through the functions of symbiotic microorganisms, thereby achieving results that unravel the evolutionary process of the cooperative environmental adaptation mechanism between the two.
Recently, the research scope has also expanded to include the advanced adaptation mechanisms of insects to spatiotemporal environmental changes, centered on seasonal variations. For example, research is underway to elucidate the components and functions of the jelly-like egg-protecting substance produced by the Japanese oak stink bug, which exhibits the unique seasonality of winter breeding, as well as the molecular and biochemical mechanisms behind the reversible body color changes in the brown-marmorated stink bug associated with overwintering diapause.
I have been fortunate enough to have cross-disciplinary experience ranging from ecology and physiology to molecular biology and biochemistry. This has given me the opportunity to focus purely on the essence of fascinating biological phenomena without being bound by the specialization of a single field. Moving forward, I aim to further advance this multifaceted research approach and unravel the ingenious mechanisms of environmental adaptation displayed by insects, which are a treasure trove of diversity.
Ochi Haruki
Associate Professor, Institute for Promotion of Medical Science, Faculty of Medicine, Yamagata University
Study on the mechanisms of gene expression regulation and their evolution in vertebrate tissue and organogenesis
Reason for winning
Member Hinagi Ochi began her research with the translational control of the transcription factor Maf in the lens, and subsequently investigated the mechanisms of muscle cell-specific gene expression by Brachyury. In recent years, by comparing the genomes of Xenopus laevis and Xenopus tropicalis, she has developed research on the evolution of cis-regulatory elements associated with whole-genome duplication. These two Xenopus species are thought to have diverged 18 million years ago, but chromosome duplication has occurred only in Xenopus laevis. Utilizing a highly efficient Xenopus transgenic system, she revealed that the divergence in expression of duplicated gene pairs in the Pax2 and Pax8 genes is brought about by the acquisition of transcriptional repression sequences. Furthermore, regarding the hand1 gene, she was able to catch a glimpse of the reality of regulatory region evolution, where a single-base substitution in the promoter sequence caused a decrease in expression in a specific tissue in one of the duplicated genes. In addition, as a new project, after identifying regeneration-signal-responsive enhancers of genes whose expression increases in response to regeneration signals, she is also proceeding with the identification of the transcription factors involved. These are significant achievements in terms of focusing on interesting phenomena and understanding the mechanisms of gene expression control. Member Ochi's research, which has effectively utilized the Xenopus transgenic system to elucidate regulation at the molecular level, is highly commendable, and further development is expected in the future. We have therefore decided to present the Zoological Society of Japan Award for Young Scientists to Member Ochi.
Winner Summary
I would like to express my gratitude for receiving the 2017 Zoological Society of Japan Award for Encouragement.
I entered this field during a time when molecular developmental biology research was thriving, marked by the creation of knockout mice leading to abnormalities in tissue and organ formation, and the transplantation of beads soaked in secreted proteins such as FGF or Shh into embryos causing dramatic morphological changes. At the time, I found it fascinating how gene expression is mechanically switched on and off to form tissues in developmental biology. Under the guidance of Professor Kunio Yasuda at the Nara Institute of Science and Technology, who was researching the regulatory mechanisms of chicken crystallin gene expression, I began my studies on gene expression regulation and development. Starting with research on the activation mechanism of the lens-specific transcription factor L-Maf in the Yasuda lab, followed by zebrafish research in Professor Monte Westerfield's lab at the University of Oregon, and Xenopus research in the Ogino lab at the Nara Institute of Science and Technology, I now lead a research laboratory at Yamagata University, where I continue to study the roles of expression regulatory mechanisms in tissue and organ formation and regeneration, as well as their evolutionary processes. Below, I introduce an overview of research that experimentally analyzed the functional transitions of cis-regulatory sequences within this context.
Vertebrates are thought to have undergone two rounds of whole-genome duplication—in which genes and their expression regulatory sequences are doubled—during their evolutionary process, with bony fish experiencing an additional one or two rounds. As a result, all genes were duplicated at least twice, meaning that the genome basically contains four copies of the same gene. Regarding the evolution of the genes themselves, numerous detailed studies have been conducted on how the extra genes generated by duplication underwent mutations and lost their functions, acquired new functions, or both duplicated genes remained in the genome with diversified expression. On the other character, although sequence comparison studies have investigated how regulatory sequences—which should have similarly doubled—have changed, there has been little research demonstrating their functions at the individual organism level. To address this issue, using diploid tropical clawed frogs and tetraploid African clawed frogs as experimental model systems for the expression diversification of duplicated genes, and through reporter transgenic analysis of gene expression regulatory regions, we have demonstrated at the individual level that the diversification of gene expression is driven not only by the acquisition of enhancers that turn gene expression on, but also by the acquisition of silencers that turn it off (Ochi et. al., Nat. Commun, 2012), and that even when not much time has passed since genome duplication, a single-nucleotide substitution is sufficient to diversify the expression of duplicated genes (Session et. al., Nature, 2016) (Ochi et. al., Dev Biol. 2017).
With the advancement of new technologies such as genome editing, research is shifting from excising and analyzing parts of traditional expression control regions to being able to modify their functions at the chromosome level. Currently, while incorporating these new technologies, I conduct experiments every day to advance research on the gene expression regulation mechanisms that govern tissue and organ formation and regeneration, as well as their evolutionary processes.
Acknowledgments
My research style and philosophy were cultivated when I was a student in the Division of Molecular Developmental Biology at the Nara Institute of Science and Technology. I would like to express my deep gratitude to Professor Emeritus Kunio Yasuda of the Nara Institute of Science and Technology and Professor Hajime Ogino, Director of the Amphibian Research Center at Hiroshima University, who taught me the fundamentals of research. I am also grateful to Professor Yoshiko Takahashi of the Faculty of Science at Kyoto University, Professor Kunio Inoue of the Faculty of Science at Kobe University, and Associate Professor Yuji Kageyama of the Faculty of Science at Kobe University for their invaluable guidance in the Division of Molecular Developmental Biology. Furthermore, I thank Professor Monte Westerfield for his guidance in developmental genetic research using zebrafish. In addition, I thank the graduate students and research assistants of the Developmental Genomics Research Group at the Nara Institute of Science and Technology and the Ochi Laboratory at the Institute for Medical Science Promotion, Yamagata University School of Medicine, who participated in and supported this research. Finally, I would like to express my sincere gratitude to Professor Akihiko Watanabe of the Faculty of Science at Yamagata University, who nominated me for this Encouragement Award, and to all the members of the Zoological Society of Japan.
Shigeru Saito
Assistant Professor, Department of Cellular Physiology, Division of Biosensing, National Institute for Physiological Sciences, Okazaki Institute for Integrative Bioscience
Elucidation of Interspecific Diversity in Temperature Sensation and Its Molecular Basis
Reason for winning
Member Shigeru Saito has consistently conducted research focusing on thermosensitive TRP channels, which act as temperature sensor molecules. Triggered by his discovery that the TRPV3 channel in the Western clawed frog exhibits thermosensitivity in the reverse direction of mammals, he advanced functional and molecular phylogenetic analyses of TRP channels across a broad range of animal species, culminating in the proposal of a hypothesis regarding the molecular evolution that generates the physiological diversity of vertebrate TRP channels. Recently, using two species of clawed frogs with different optimal temperatures, he has also developed comparative physiological and ecological research, revealing that interspecies differences in the thermosensitivity of TRP channels are closely related to differences in optimal temperatures at the individual level. Centered on interspecies comparison, which is indispensable to zoology, Member Saito's research—which clearly demonstrates the connection between molecular-level changes in TRP channels and the diversification of thermosensitivity—is highly evaluated. Because it holds promise for further development into the more general study of the molecular basis for acquiring environmental adaptation capabilities, it was decided to award the Zoological Society of Japan Award for Young Scientists to Member Saito.
Winner Summary
Temperature is an environmental factor that can even dictate survival, and animals have developed a physiological mechanism known as "temperature sensation" to accurately perceive external temperatures and body temperature. As various animal species adapted to environments with different temperature conditions, one might imagine, for example, that species inhabiting hot environments became less sensitive to "heat" than species inhabiting cool environments. I am intrigued by questions such as how much the mechanisms by which animals sense temperature have changed over the course of evolution, and how such changes have related to the environmental adaptation of each animal species. Therefore, I have isolated temperature-sensitive TRP channels, which act as sensor molecules for temperature reception mechanisms, from various animal species and compared them using a combination of molecular evolutionary and electrophysiological approaches. In this paper, I introduce the main results obtained so far.
- temperature sensitivityTRPfunctional diversity of channels and its evolutionary process
Temperature-sensitive TRP channels are sensor molecules expressed in sensory nerves and other tissues, and are activated by temperature stimuli. These channels possess multimodal properties, being activated not only by physical stimuli other than temperature but also by various chemical substances. Among them, TRPA1 and TRPV1 are involved in the reception of temperature stimuli perceived as pain and of irritant chemicals. To investigate the evolutionary dynamics of molecules responsible for such similar physiological mechanisms, we performed a comparative analysis among vertebrate species. TRPA1 from amphibians (Western clawed frog), birds (chicken), and reptiles (green anole lizard) were activated by multiple irritant chemicals, similarly to their mammalian orthologs (Saito et al. 2012, 2014). However, their temperature responsiveness differed significantly from that of mammals. While mammalian TRPA1 has been reported to be activated by low temperatures, the three newly analyzed TRPA1s were activated not by low temperatures, but by high-temperature stimuli. On the other hand, TRPV1, which is involved in the reception of high-temperature ranges in mammals, birds, and fish, possessed similar properties in the Western clawed frog (Ohkita and Saito et al. 2012).
Previous studies estimate that TRPA1 emerged in the early stages of the animal evolutionary lineage and acquired sensitivity to high temperatures and chemicals. On the other hand, our molecular phylogenetic analysis shows that TRPV1 is a newly emerged gene in the evolutionary lineage of vertebrate species (Saito et al. 2006, 2011). It is suggested that the acquisition of TRPV1 as a high-temperature sensor in the ancestral species of vertebrates relaxed the evolutionary constraints on the heat sensitivity of TRPA1, acting as a factor for the variation of temperature sensitivity among species (Saito and Tominaga 2015).
- temperature sensitivityTRPmolecular basis underlying the functional interspecies differences of channels
In the course of functional analysis of chicken TRPA1, we found that this channel is activated by methyl anthranilate (MA), a bird repellent, and demonstrated for the first time that bird avoidance behavior induced by MA is a phenomenon mediated by this channel (Saito et al. 2014). When MA was applied to TRPA1 from five vertebrate species, its activity varied among species. Through amino acid substitution pattern analysis of TRPA1 and screening of mutant channels, we identified three amino acid residues involved in activation by MA. Furthermore, we have advanced the identification of the molecular basis for the activation and inhibition of temperature-sensitive TRP channels utilizing interspecies diversity by identifying amino acid residues responsible for the interspecies differences in the sensitivity of TRPV1 to capsaicin (Ohkita and Saito et al. 2012; Saito et al. 2016) and those involved in the action of TRPA1 inhibitors expected to be used as analgesics (Gupta et al. 2016).
- Related to temperature adaptationTRPEvolution of channel features
To elucidate the evolutionary changes in temperature sensation involved in environmental adaptation and their molecular basis, comparative analyses of two Xenopus species with different optimal temperatures were conducted. Xenopus tropicalis and Xenopus laevis have different distribution ranges, and the latter is adapted to cooler environments. Comparing the responsiveness to high-temperature stimulation between the two species revealed that Xenopus laevis has higher sensitivity to high temperatures at both behavioral and sensory nerve levels. Next, the channel properties of TRPA1 and TRPV1, which are high-temperature sensors, were compared. It was found that Xenopus laevis TRPA1 has higher activity in response to high-temperature stimulation than that of Xenopus tropicalis, and furthermore, is activated at lower temperatures. In addition, the temperature response characteristics of TRPV1 also differed between the two species, and it was further demonstrated that three amino acid substitutions are involved in the species differences in the high-temperature responsiveness of this channel (Saito et al. 2016; Saito and Tominaga 2017). Although the temperature reception mechanism is a complex system involving countless proteins ranging from the peripheral nervous system to the central nervous system, it was suggested that simple functional changes in peripheral sensor molecules have driven the evolutionary changes in temperature sensation and the organism-level behavioral responses based on it.
Through comparative analyses among vertebrate species, our previous research has revealed that changes in the function of temperature-sensitive TRP channels have driven dynamic shifts in thermosensation and chemosensation. However, because ecologically and physiologically characteristics differ markedly among distantly related species, it has been difficult to establish a clear link between changes in temperature sensor molecules and environmental adaptation. Therefore, we are currently focusing on comparative analyses among closely related species or within species that exhibit differences in temperature-related traits. Through such analyses, we aim to elucidate the evolutionary mechanisms of thermosensation in greater detail and, furthermore, to develop research that connects molecular-level evolutionary changes with species-specific ecological traits.
