Updated on 2025/05/09

Information

 

写真a

 
HOSOKAWA TAKAHIRO
 
Organization
Faculty of Science Department of Biology Associate Professor
School of Sciences Department of Biology(Concurrent)
Graduate School of Systems Life Sciences Department of Systems Life Sciences(Concurrent)
Title
Associate Professor
External link

Degree

  • Ph. D. ( 2003.3 Kyushu University )

Research Interests・Research Keywords

  • Research theme: Parent-offspring interaction in insects

    Keyword: behavior, biodiversity

    Research period: 2019.4

  • Research theme: Interaction between insects and symbiotic microorganisms

    Keyword: behavior, coevolution, biodiversity

    Research period: 2014.9

Awards

  • 沖縄研究奨励賞

    2019.1   公益財団法人沖縄協会   琉球列島の昆虫共生微生物の多様性に関する研究

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    体内に共生細菌を保持し、共生細菌と絶対的相利共生関係を築いている生物は多い。その進化過程はこれまで不明であったが、本研究では野外昆虫集団において現在進行中の進化として捉えることに成功した。また、進化段階の異なるさまざまな共生細菌が存在するというダイナミックな進化過程が琉球列島の昆虫集団のみで見られることも発見し、琉球列島の生物多様性のこれまで知られていなかった新しい側面を明らかにした。

  • 2015年日本応用動物昆虫学会論文賞

    2015.3   日本応用動物昆虫学会   Tada A., Kikuchi Y., Hosokawa T., Musolin D. L., Fujisaki K., Fukatsu T. (2011) Obligate association with gut bacterial symbiont in Japanese populations of the southern green stinkbug Nezara viridula (Heteroptera: Pentatomidae). Applied Entomology and Zoology 46: 483-488.

  • 平成26年度産総研論文賞

    2014.11   産業技術総合研究所   Kikuchi Y., Hayatsu M., Hosokawa T., Nagayama A., Tago K., Fukatsu T. (2012) Symbiont-mediated insecticide resistance. Proceedings of the National Academy of Sciences of the United States of America 109: 8618-8622.

Papers

  • Relevance of microbial symbiosis to insect behavior Reviewed

    Takahiro Hosokawa, Takema Fukatsu

    Current Opinion in Insect Science   39   91 - 100   2020.6

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    Authorship:Lead author, Corresponding author   Language:English   Publishing type:Research paper (scientific journal)  

    Microbial symbiosis is widespread among insects. This article reviews our understanding of insect behaviors relevant to commensalistic and mutualistic microbial symbiosis, which has received relatively less attention compared to insect behaviors in parasitic symbiosis. First, we review our knowledge of symbiont transmission behaviors by which the host insects maintain associations with beneficial microorganisms over generations. Some insects that extracellularly harbor mutualistic symbionts exhibit particularly sophisticated behaviors for vertical symbiont transmission. Next, we highlight notable studies on behavioral changes induced by symbiont infection. In the last decade, a number of studies have demonstrated or suggested that mutualistic or commensalistic symbiont infections affect their host behaviors. Finally, future directions regarding these research topics are discussed.

    DOI: 10.1016/j.cois.2020.03.004

  • Obligate bacterial mutualists evolving from environmental bacteria in natural insect populations Reviewed

    Takahiro Hosokawa, Yoshiko Ishii, Naruo Nikoh, Manabu Fujie, Nori Satoh, Takema Fukatsu

    Nature Microbiology   1 ( 1 )   2016.1

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    Authorship:Lead author   Language:English   Publishing type:Research paper (scientific journal)  

    Diverse organisms are associated with obligate microbial mutualists. How such essential symbionts have originated from free-living ancestors is of evolutionary interest. Here we report that, in natural populations of the stinkbug Plautia stali, obligate bacterial mutualists are evolving from environmental bacteria. Of six distinct bacterial lineages associated with insect populations, two are uncultivable with reduced genomes, four are cultivable with non-reduced genomes, one uncultivable symbiont is fixed in temperate populations, and the other uncultivable symbiont coexists with four cultivable symbionts in subtropical populations. Symbiont elimination resulted in host mortality for all symbionts, while re-infection with any of the symbionts restored normal host growth, indicating that all the symbionts are indispensable and almost equivalent functionally. Some aseptic newborns incubated with environmental soils acquired the cultivable symbionts and normal growth was restored, identifying them as environmental Pantoea spp. Our finding uncovers an evolutionary transition from a free-living lifestyle to obligate mutualism that is currently ongoing in nature.

    DOI: 10.1038/nmicrobiol.2015.11

  • Uncultivable and cultivable gut symbiotic bacteria of the jewel stinkbug <i>Scutellera amethystina</i> (Hemiptera: Scutelleridae)

    Hosokawa, T; Moriyama, M; Koga, R; Fukatsu, T

    APPLIED ENTOMOLOGY AND ZOOLOGY   60 ( 2 )   151 - 157   2025.5   ISSN:0003-6862 eISSN:1347-605X

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    Publisher:Applied Entomology and Zoology  

    Many plant-sucking stinkbugs develop a symbiotic organ in a posterior region of the midgut, wherein specific symbiotic bacteria exist and contribute to survival and reproduction of their hosts. The symbiotic bacteria range from uncultivable ones that have lost the capability of proliferation without their hosts to cultivable ones that retain the ability to proliferate not only within their hosts but also in the external environment. Such diverse host–symbiont relationships seem to represent different evolutionary stages from free-living through facultative symbiosis to obligatory mutualism. However, our understanding of such evolutionary processes toward symbiosis is still limited. Here we investigated the gut symbiotic bacteria of the invasive jewel stinkbugs Scutellera amethystina (Germar) (Hemiptera: Scutelleridae) collected from different subtropical island populations in Japan. While most insects were associated with a specific Pantoea-allied uncultivable bacterial symbiont in the midgut symbiotic organ, we found an insect associated with a phylogenetically distinct Pantoea symbiont, which was cultivable and closely related to cultivable gut symbiotic bacteria previously reported from other stinkbug species. These results uncover intraspecific coexistence of uncultivable and cultivable gut symbiotic bacteria in S. amethystina, which provides insights into the evolutionary processes toward obligatory mutualism and symbiont uncultivability.

    DOI: 10.1007/s13355-025-00897-w

    Web of Science

    Scopus

  • The burrower bug Macroscytus japonensis (Hemiptera: Cydnidae) acquires obligate symbiotic bacteria from the environment. Reviewed

    Nakawaki T., Watanabe S., Hosokawa T.

    Zoological Letters   10   15   2024.8

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    Authorship:Last author, Corresponding author   Language:English   Publishing type:Research paper (scientific journal)  

    DOI: https://doi.org/10.1186/s40851-024-00238-9

  • Defensive fungal symbiosis on insect hindlegs.

    Nishino T, Mukai H, Moriyama M, Hosokawa T, Tanahashi M, Tachikawa S, Nikoh N, Koga R, Fukatsu T

    bioRxiv : the preprint server for biology   2024.3

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    Language:English  

    DOI: 10.1101/2024.03.25.586038

    PubMed

  • Protective function of maternal care against egg predators in the shield bug Sastragala esakii (Hemiptera: Acanthosomatidae) Reviewed International journal

    #Nishimura K., @Kudo S., Hosokawa T.

    Entomological Science   26 ( 3 )   e12555   2023.6

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    Authorship:Last author, Corresponding author   Language:Japanese   Publishing type:Research paper (scientific journal)  

    DOI: https://doi.org/10.1111/ens.12555

  • Potential impact of <i>Leptoglossus occidentalis</i> on <i>Pinus thunbergii</i> seed production

    Matsunaga Koji, Iwaizumi Masakazu G, Kubota Masahiro, Hara Ryotaro, Kitajima Ryotaro, Hosokawa Takahiro, Watanabe Atsushi, Kume Atsushi

    The Japanese Forest Society Congress   134 ( 0 )   1   2023.5

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    Language:English   Publisher:THE JAPANESE FORESTRY SOCIETY  

    <p>[in Japanese]</p>

    DOI: 10.11519/jfsc.134.0_1

    CiNii Research

  • Population dynamics of <i>Leptoglossus occidentalis</i> in Koshi City, Kumamoto Prefecture

    Hara Ryotaro, Matsunaga Koji, Watanabe Atsushi, Hosokawa Takahiro, Kume Atsushi

    The Japanese Forest Society Congress   134 ( 0 )   4   2023.5

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    Language:English   Publisher:THE JAPANESE FORESTRY SOCIETY  

    <p>[in Japanese]</p>

    DOI: 10.11519/jfsc.134.0_4

    CiNii Research

  • Spiroplasma as facultative bacterial symbionts of stinkbugs Reviewed International journal

    Kakizawa S., Hosokawa T., Oguchi K., Miyakoshi K., Fukatsu T.

    Frontiers in Microbiology   13 ( 1044771 )   2022.10

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    Language:English   Publishing type:Research paper (scientific journal)  

    DOI: 10.3389/fmicb.2022.1044771

  • Intercontinental diversity of Caballeronia gut symbionts in the conifer pest bug Leptoglossus occidentalis Reviewed International journal

    Ohbayashi T., Cossard R., Lextrait G., Hosokawa T., Lesieur V., Takeshita K., Tago K., Mergaert P., Kikuchi Y.

    Microbes and Environments   33 ( 3 )   2022.8

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    Language:English   Publishing type:Research paper (scientific journal)  

    DOI: https://doi.org/10.1264/jsme2.ME22042

  • Single mutation makes Escherichia coli an insect mutualist Invited Reviewed International journal

    Koga, Ryuichi; Moriyama, Minoru; Onodera-Tanifuji, Naoko; Ishii, Yoshiko; Takai, Hiroki; Mizutani, Masaki; Oguchi, Kohei; Okura, Reiko; Suzuki, Shingo; Gotoh, Yasuhiro; Hayashi, Tetsuya; Seki, Masahide; Suzuki, Yutaka; Nishide, Yudai; Hosokawa, Takahiro; Wakamoto, Yuichi; Furusawa, Chikara; Fukatsu, Takema

    NATURE MICROBIOLOGY   7 ( 8 )   1141 - +   2022.8

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    Language:English   Publishing type:Research paper (scientific journal)  

    DOI: 10.1038/s41564-022-01179-9

  • Seed production reduction in <i>Pinus thunbergii</i> caused by <i>Leptoglossus occidentalis</i>

    Matsunaga Koji, Fukatsu Eitaro, Iwaizumi Masakazu G, Kubota Masahiro, Hara Ryotaro, Kitajima Ryotaro, Hosokawa Takahiro, Watanabe Atsushi, Kume Atsushi

    The Japanese Forest Society Congress   133 ( 0 )   159   2022.5

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    Language:English   Publisher:THE JAPANESE FORESTRY SOCIETY  

    <p>[in Japanese]</p>

    DOI: 10.11519/jfsc.133.0_159

    CiNii Research

  • Monitoring <i>Leptoglossus occidentalis</i> in young black pine stands in Koshi City, Kumamoto Prefecture

    Hara Ryotaro, Matsunaga Koji, Watanabe Atsushi, Hosokawa Takahiro, Kitajima Ryotaro, Kume Atsushi

    The Japanese Forest Society Congress   133 ( 0 )   198   2022.5

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    Language:English   Publisher:THE JAPANESE FORESTRY SOCIETY  

    <p>[in Japanese]</p>

    DOI: 10.11519/jfsc.133.0_198

    CiNii Research

  • Host’s guardian protein counters degenerative symbiont evolution Reviewed International journal

    Koga R., Tanahashi M., Nikoh N., Hosokawa T., Meng X. Y., Moriyama M., Fukatsu T.

    Proceedings of the National Academy of Sciences of the United States of America   118 ( 25 )   e2103957118   2021.6

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    DOI: https://doi.org/10.1073/pnas.2103957118

  • Environmental acquisition of gut symbiotic bacteria in the saw-toothed stinkbug Megymenum gracilicorne (Hemiptera: Pentatomoidea: Dinidoridae) Reviewed International journal

    Nishino T., Hosokawa T., Meng X. Y., Koga R., Moriyama M., Fukatsu T.

    Zoological Science   38 ( 3 )   213 - 222   2021.2

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    DOI: https://doi.org/10.2108/zs200163

  • Reduced Genome of the Gut Symbiotic Bacterium "Candidatus Benitsuchiphilus tojoi" Provides Insight Into Its Possible Roles in Ecology and Adaptation of the Host Insect Reviewed International journal

    Mondal S. I., Akter A., Koga R., Hosokawa T., Dayi M., Murase K., Tanaka R., Shigenobu S., Fukatsu T., Kikuchi T.

    Frontiers in Microbiology   11   840   2020.5

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    Diverse animals, including insects, harbor microbial symbionts within their gut, body cavity, or cells. The subsocial parastrachiid stinkbug Parastrachia japonensis is well-known for its peculiar ecological and behavioral traits, including its prolonged non-feeding diapause period and maternal care of eggs/nymphs in an underground nest. P. japonensis harbors a specific bacterial symbiont within the gut cavity extracellularly, which is vertically inherited through maternal excretion of symbiont-containing white mucus. Thus far, biological roles of the symbiont in the host lifecycle has been little understood. Here we sequenced the genome of the uncultivable gut symbiont "Candidatus Benitsuchiphilus tojoi." The symbiont has an 804 kb circular chromosome encoding 606 proteins and a 14.5 kb plasmid encoding 13 proteins. Phylogenetic analysis indicated that the bacterium is closely related to other obligate insect symbionts belonging to the Gammaproteobacteria, including Buchnera of aphids and Blochmannia of ants, and the most closely related to Ishikawaella, an extracellular gut symbiont of plataspid stinkbugs. These data suggested that the symbiont genome has evolved like highly reduced gamma-proteobacterial symbiont genomes reported from a variety of insects. The presence of genes involved in biosynthesis pathways for amino acids, vitamins, and cofactors in the genome implicated the symbiont as a nutritional mutualist, supplementing essential nutrients to the host. Interestingly, the symbiont's plasmid encoded genes for thiamine and carotenoid synthesis pathways, suggesting the possibility of additional functions of the symbiont for protecting the host against oxidative stress and DNA damage. Finally, possible involvement of the symbiont in uric acid metabolism during diapause is discussed.

    DOI: 10.3389/fmicb.2020.00840

  • Diversity and evolution of bacterial symbionts in the gut symbiotic organ of jewel stinkbugs (Hemiptera Scutelleridae) Reviewed

    Takahiro Hosokawa, Megumi Imanishi, Ryuichi Koga, Takema Fukatsu

    Applied Entomology and Zoology   54 ( 4 )   359 - 367   2019.11

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    The majority of plant-sucking stinkbugs of the superfamily Pentatomoidea possess numerous crypts in the midgut as the symbiotic organ, where specific and beneficial symbiotic bacteria are harbored extracellularly. The host–symbiont relationships are co-speciating in the families Plataspidae, Acanthosomatidae and Urostylididae, but promiscuous in the families Pentatomidae and Cydnidae. As for the family Scutelleridae, only a few species have been examined for their gut symbiotic bacteria. Here, we comprehensively investigated Japanese scutellerid stinkbugs representing 6 genera, 8 species, and 24 individuals. Molecular phylogenetic analysis revealed that the scutellerid gut symbionts are polyphyletic, consisting of at least seven distinct phylogenetic groups in the Gammaproteobacteria. In four of the seven groups, the symbionts were closely related to each other, to the pentatomid gut symbionts, and to environmental bacteria of the genus Pantoea. These results strongly suggest that the scutellerid gut symbionts are of multiple evolutionary origins, presumably entailing repeated symbiont acquisitions, replacements and/or horizontal transfers in a promiscuous manner. Elimination of the gut symbionts from Lampromicra miyakona resulted in high mortality without adult emergence, confirming that the gut symbionts are of beneficial nature. In conclusion, the host–symbiont associations in the Scutelleridae seem to be similar to those in the Pentatomidae and Cydnidae.

    DOI: 10.1007/s13355-019-00630-4

  • Small genome symbiont underlies cuticle hardness in beetles Reviewed

    Hisashi Anbutsu, Minoru Moriyama, Naruo Nikoh, Takahiro Hosokawa, Ryo Futahashi, Masahiko Tanahashi, Xian Ying Meng, Takashi Kuriwada, Naoki Mori, Kenshiro Oshima, Masahira Hattori, Manabu Fujie, Noriyuki Satoh, Taro Maeda, Shuji Shigenobu, Ryuichi Koga, Takema Fukatsu

    Proceedings of the National Academy of Sciences of the United States of America   114 ( 40 )   E8382 - E8391   2017.10

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    Beetles, representing the majority of the insect species diversity, are characterized by thick and hard cuticle, which plays important roles for their environmental adaptation and underpins their inordinate diversity and prosperity. Here, we report a bacterial endosymbiont extremely specialized for sustaining beetle’s cuticle formation. Many weevils are associated with a γ-proteobacterial endosymbiont lineage Nardonella, whose evolutionary origin is estimated as older than 100 million years, but its functional aspect has been elusive. Sequencing of Nardonella genomes from diverse weevils unveiled drastic size reduction to 0.2 Mb, in which minimal complete gene sets for bacterial replication, transcription, and translation were present but almost all of the other metabolic pathway genes were missing. Notably, the only metabolic pathway retained in the Nardonella genomes was the tyrosine synthesis pathway, identifying tyrosine provisioning as Nardonella’s sole biological role. Weevils are armored with hard cuticle, tyrosine is the principal precursor for cuticle formation, and experimental suppression of Nardonella resulted in emergence of reddish and soft weevils with low tyrosine titer, confirming the importance of Nardonella-mediated tyrosine production for host’s cuticle formation and hardening. Notably, Nardonella’s tyrosine synthesis pathway was incomplete, lacking the final step transaminase gene. RNA sequencing identified host’s aminotransferase genes up-regulated in the bacteriome. RNA interference targeting the aminotransferase genes induced reddish and soft weevils with low tyrosine titer, verifying host’s final step regulation of the tyrosine synthesis pathway. Our finding highlights an impressively intimate and focused aspect of the host–symbiont metabolic integrity via streamlined evolution for a single biological function of ecological relevance.

    DOI: 10.1073/pnas.1712857114

  • Obligate gut symbiotic association in the sloe bug Dolycoris baccarum (Hemiptera Pentatomidae) Reviewed

    Hideomi Itoh, Yu Matsuura, Takahiro Hosokawa, Takema Fukatsu, Yoshitomo Kikuchi

    Applied Entomology and Zoology   52 ( 1 )   51 - 59   2017.2

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    A number of phytophagous stinkbugs are associated with specific bacterial symbionts in their alimentary tracts. The sloe bug Dolycoris baccarum (Linnaeus), a notorious pest of diverse crops, possesses a number of sac-like tissues, called crypts, in a posterior section of the midgut, wherein a specific bacterial symbiont colonizes. Here we characterized the symbiotic bacterium of D. baccarum by histological analysis, molecular phylogeny, and diagnostic PCR with a specific primer set. The cloning and sequencing analyses of bacterial 16S rRNA genes and fluorescent in situ hybridization demonstrated that the sloe bug is associated with a single species of Gammaproteobacteria in the midgut crypts. Molecular phylogenetic analysis strongly suggested that the symbiont should be placed in the genus Pantoea of the Enterobacteriaceae. Diagnostic PCR and egg surface sterilization with formalin indicated the stinkbug vertically transmits the Pantoea symbiont via egg-smearing. The sterilization-produced aposymbiotic nymphs showed high mortality and no insects reached adulthood. In addition, the Pantoea symbiont was uncultivable outside the insect host, indicating an obligate and intimate host-symbiont association.

    DOI: 10.1007/s13355-016-0453-0

  • Collapse of insect gut symbiosis under simulated climate change Reviewed

    Yoshitomo Kikuchi, Akiyo Tada, Dmitry L. Musolin, Nobuhiro Hari, Takahiro Hosokawa, Kenji Fujisaki, Takema Fukatsu

    mBio   7 ( 5 )   2016.9

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    Global warming impacts diverse organisms not only directly but also indirectly via other organisms with which they interact. Recently, the possibility that elevated temperatures resulting from global warming may substantially affect biodiversity through disrupting mutualistic/parasitic associations has been highlighted. Here we report an experimental demonstration that global warming can affect a pest insect via suppression of its obligate bacterial symbiont. The southern green stinkbug Nezara viridula depends on a specific gut bacterium for its normal growth and survival. When the insects were reared inside or outside a simulated warming incubator wherein temperature was controlled at 2.5°C higher than outside, the insects reared in the incubator exhibited severe fitness defects (i.e., retarded growth, reduced size, yellowish body color, etc.) and significant reduction of symbiont population, particularly in the midsummer season, whereas the insects reared outside did not. Rearing at 30°C or 32.5°C resulted in similar defective phenotypes of the insects, whereas no adult insects emerged at 35°C. Notably, experimental symbiont suppression by an antibiotic treatment also induced similar defective phenotypes of the insects, indicating that the host’s defective phenotypes are attributable not to the heat stress itself but to the suppression of the symbiont population induced by elevated temperature. These results strongly suggest that high temperature in the midsummer season negatively affects the insects not directly but indirectly via the heat-vulnerable obligate bacterial symbiont, which highlights the practical relevance of mutualism collapse in this warming world.

    DOI: 10.1128/mBio.01578-16

  • Suppression of bedbug's reproduction by RNA interference of vitellogenin Reviewed

    Minoru Moriyama, Takahiro Hosokawa, Masahiko Tanahashi, Naruo Nikoh, Takema Fukatsu

    PloS one   11 ( 4 )   2016.4

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    Recent resurgence of the bedbug Cimex lectularius is a global problem on the public health. On account of the worldwide rise of insecticide-resistant bedbug populations, exploration of new approaches to the bedbug control and management is anticipated. In this context, gene silencing by RNA interference (RNAi) has been considered for its potential application to pest control and management, because RNAi enables specific suppression of target genes and thus flexible selection of target traits to be disrupted. In this study, in an attempt to develop a control strategy targeting reproduction of the bedbug, we investigated RNAimediated gene silencing of vitellogenin (Vg), a major yolk protein precursor essential for oogenesis. From the bedbug transcriptomes, we identified a typical Vg gene and a truncated Vg gene, which were designated as ClVg and ClVg-like, respectively. ClVg gene was highly expressed mainly in the fat body of adult females, which was more than 100 times higher than the expression level of ClVg-like gene, indicating that ClVg gene is the primary functional Vg gene in the bedbug. RNAi-mediated suppression of ClVg gene expression in adult females resulted in drastically reduced egg production, atrophied ovaries, and inflated abdomen due to hypertrophied fat bodies. These phenotypic consequences are expected not only to suppress the bedbug reproduction directly but also to deteriorate its feeding and survival indirectly via behavioral modifications. These results suggest the potential of ClVg gene as a promising target for RNAi-based population management of the bedbug.

    DOI: 10.1371/journal.pone.0153984

  • Riboflavin provisioning underlies wolbachia’s fitness contribution to its insect host Reviewed

    Minoru Moriyama, Naruo Nikoh, Takahiro Hosokawa, Takema Fukatsu

    mBio   6 ( 6 )   2015.11

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    Endosymbiotic bacteria of the genus Wolbachia represent the most successful symbiotic bacteria in the terrestrial ecosystem. The success of Wolbachia has been ascribed to its remarkable phenotypic effects on host reproduction, such as cytoplasmic incompatibility, whereby maternally inherited bacteria can spread in their host populations at the expense of their host’s fitness. Meanwhile, recent theoretical as well as empirical studies have unveiled that weak and/or conditional positive fitness effects may significantly facilitate invasion and spread of Wolbachia infections in host populations. Here, we report a previously unrecognized nutritional aspect, the provision of riboflavin (vitamin B2), that potentially underpins the Wolbachia-mediated fitness benefit to insect hosts. A comparative genomic survey for synthetic capability of B vitamins revealed that only the synthesis pathway for riboflavin is highly conserved among diverse insect-associated Wolbachia strains, while the synthesis pathways for other B vitamins were either incomplete or absent. Molecular phylogenetic and genomic analyses of riboflavin synthesis genes from diverse Wolbachia strains revealed that, in general, their phylogenetic relationships are concordant with Wolbachia’s genomic phylogeny, suggesting that the riboflavin synthesis genes have been stably maintained in the course of Wolbachia evolution. In rearing experiments with bedbugs (Cimex lectularius) on blood meals in which B vitamin contents were manipulated, we demonstrated that Wolbachia’s riboflavin provisioning significantly contributes to growth, survival, and reproduction of the insect host. These results provide a physiological basis upon which Wolbachia-mediated positive fitness consequences are manifested and shed new light on the ecological and evolutionary relevance of Wolbachia infections. IMPORTANCE Conventionally, Wolbachia has been regarded as a parasitic bacterial endosymbiont that manipulates the host insect’s reproduction in a selfish manner, which tends to affect a host’s fitness negatively. Meanwhile, some theories predict that, at the same time, Wolbachia can directly affect the host’s fitness positively, which may potentially reconcile the negative effect and facilitate spread and stability of the symbiotic association. Here we demonstrate, by using comparative genomic and experimental approaches, that among synthetic pathways for B vitamins, the synthetic pathway for riboflavin (vitamin B2) is exceptionally conserved among diverse insect-associated Wolbachia strains, and Wolbachia’s riboflavin provisioning certainly contributes to growth, survival, and reproduction in an insect. These findings uncover a nutritional mechanism of a Wolbachia-mediated fitness benefit, which provides empirical evidence highlighting a “Jekyll and Hyde” aspect of Wolbachia infection.

    DOI: 10.1128/mBio.01732-15

  • Nardonella endosymbionts of Japanese pest and non-pest weevils (Coleoptera Curculionidae) Reviewed

    Takahiro Hosokawa, Ryuichi Koga, Kohjiro Tanaka, Minoru Moriyama, Hisashi Anbutsu, Takema Fukatsu

    Applied Entomology and Zoology   50 ( 2 )   223 - 229   2015.5

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    Many weevils are known as notorious devastating agricultural pests and generally associated with symbiotic bacteria. Here, we investigated the following pest and non-pest weevils collected in Japan for their bacterial associates: the banana stem weevil Odoiporus longicollis (Olivier); the Asiatic palm weevil Rhabdoscelus lineaticollis (Heller); the red palm weevil Rhynchophorus ferrugineus (Olivier); the Japanese giant weevil Sipalinus gigas (Fabricius); the olive weevil Pimelocerusperforatus (Roelofs); the black hard weevil Pachyrhynchus infernalis Fairmaire; and the Yonaguni hard weevil Metapocyrtus yonagunianus Chujo. Bacterial 16S rRNA gene was amplified by a polymerase chain reaction (PCR) from all the weevils, and genotyping and sequencing of the PCR products revealed that Nardonella, an ancient weevil-associated endosymbiont lineage, is the dominant bacterial associate for them. Molecular phylogenetic analyses based on bacterial 16S rRNA and groEL gene sequences showed that the weevil endosymbionts are placed within the Nardonella clade in the γ-Proteobacteria. The phylogenetic relationship of the Nardonella endosymbionts was concordant with the systematics of the weevil hosts, favoring the hypothesis of weevil-Nardonella co-speciation over evolutionary time. In situ hybridization visualized localization of the Nardonella endosymbionts in the larval bacteriome at the foregut-midgut junction in R. ferrugineus and S. gigas, and in the ovarial tips of adult females in O. longicollis. Our results highlight the general relevance of the Nardonella endosymbionts to the biology, control and management of these and other pest weevils.

    DOI: 10.1007/s13355-015-0326-y

  • Female-specific specialization of a posterior end region of the midgut symbiotic organ in Plautia splendens and allied stinkbugs Reviewed

    Toshinari Hayashi, Takahiro Hosokawa, Xian Ying Meng, Ryuichi Koga, Takema Fukatsu

    Applied and environmental microbiology   81 ( 7 )   2603 - 2611   2015.1

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    Many stinkbugs (Insecta: Hemiptera: Heteroptera) are associated with bacterial symbionts in a posterior region of the midgut. In these stinkbugs, adult females excrete symbiont-containing materials from the anus for transmission of the beneficial symbionts to their offspring. For ensuring the vertical symbiont transmission, a variety of female-specific elaborate traits at the cellular, morphological, developmental, and behavioral levels have been reported from diverse stinkbugs of the families Plataspidae, Urostylididae, Parastrachiidae, etc. Meanwhile, such elaborate female-specific traits for vertical symbiont transmission have been poorly characterized for the largest and economically important stinkbug family Pentatomidae. Here, we investigated the midgut symbiotic system of a pentatomid stinkbug, Plautia splendens. A specific gammaproteobacterial symbiont was consistently present extracellularly in the cavity of numerous crypts arranged in four rows on the midgut fourth section. The symbiont was smeared on the egg surface upon oviposition by adult females, orally acquired by newborn nymphs, and thereby transmitted vertically to the next generation and important for growth and survival of the host insects. We found that, specifically in adult females, several rows of crypts at the posterior end region of the symbiotic midgut were morphologically differentiated and conspicuously enlarged, often discharging the symbiotic bacteria from the crypt cavity to the main tract of the symbiotic midgut. The female-specific enlarged end crypts were also found in other pentatomid stinkbugs Plautia stali and Carbula crassiventris. These results suggest that the enlarged end crypts represent a female-specific specialized morphological trait for vertical symbiont transmission commonly found among stinkbugs of the family Pentatomidae.

    DOI: 10.1128/AEM.04057-14

  • Symbiont-supplemented maternal investment underpinning host's ecological adaptation Reviewed

    Nahomi Kaiwa, Takahiro Hosokawa, Naruo Nikoh, Masahiko Tanahashi, Minoru Moriyama, Xian Ying Meng, Taro Maeda, Katsushi Yamaguchi, Shuji Shigenobu, Motomi Ito, Takema Fukatsu

    Current Biology   24 ( 20 )   2465 - 2470   2014.10

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    Maternal investment for offspring's growth and survival is widespread among diverse organisms [1-3]. Vertical symbiont transmission via maternal passage is also pivotal for offspring's growth and survival in many organisms [4-6]. Hence, it is expected that vertical symbiont transmission may coevolve with various organismal traits concerning maternal investment in offspring. Here we report a novel phenotypic syndrome entailing morphological, histological, behavioral, and ecological specializations for maternal investment and vertical symbiont transmission in stinkbugs of the family Urostylididae [7-9]. Adult females develop huge ovaries exaggerated for polysaccharide excretion, possess novel ovipositor-associated organs for vertical transmission of a bacterial symbiont ("Candidatus Tachikawaea gelatinosa"), and lay eggs covered with voluminous symbiont- supplemented jelly. Newborns hatch in midwinter, feed solely on the jelly, acquire the symbiont, and grow during winter. In spring, the insects start feeding on plant sap, wherein the symbiont localizes to a specializedmidgut region and supplies essential amino acids deficient in the host's diet. The reduced symbiont genome and host-symbiont cospeciation indicate their obligate association over evolutionary time. Experimental deprivation of the jelly results in nymphal mortality, whereas restoration of the jelly leads to recovered nymphal growth, confirming that the jelly supports nymphal growth in winter. Chemical analyses demonstrate that the galactan-based jelly contains a sufficient quantity of amino acids to sustain nymphal growth to the third instar. The versatile biological roles of the symbiont-containing eggcovering jelly highlight intricate evolutionary interactions between maternal resource investment and vertical symbiont transmission, which are commonly important for offspring's growth, survival, and ecological adaptation.

    DOI: 10.1016/j.cub.2014.08.065

  • Evolutionary origin of insect-Wolbachia nutritional mutualism Reviewed

    Naruo Nikoh, Takahiro Hosokawa, Minoru Moriyama, Kenshiro Oshima, Masahira Hattori, Takema Fukatsu

    Proceedings of the National Academy of Sciences of the United States of America   111 ( 28 )   10257 - 10262   2014.7

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    Obligate insect-bacterium nutritional mutualism is among the most sophisticated forms of symbiosis, wherein the host and the symbiont are integrated into a coherent biological entity and unable to survive without the partnership. Originally, however, such obligate symbiotic bacteria must have been derived from free-living bacteria. How highly specialized obligate mutualisms have arisen from less specialized associations is of interest. Here we address this evolutionary issue by focusing on an exceptional insect-Wolbachia nutritional mutualism. Although Wolbachia endosymbionts are ubiquitously found in diverse insects and generally regarded as facultative/parasitic associates for their insect hosts, a Wolbachia strain associated with the bedbug Cimex lectularius, designated as wCle, was shown to be essential for host's growth and reproduction via provisioning of B vitamins. We determined the 1,250,060-bp genome of wCle, which was generally similar to the genomes of insect-associated facultative Wolbachia strains, except for the presence of an operon encoding the complete biotin synthetic pathway that was acquired via lateral gene transfer presumably from a coinfecting endosymbiont Cardinium or Rickettsia. Nutritional and physiological experiments, in which wCle-infected and wCle-cured bedbugs of the same genetic background were fed on B-vitamin-manipulated blood meals via an artificial feeding system, demonstrated that w Cle certainly synthesizes biotin, and the wCle-provisioned biotin significantly contributes to the host fitness. These findings strongly suggest that acquisition of a single gene cluster consisting of biotin synthesis genes underlies the bedbug-Wolbachia nutritional mutualism, uncovering an evolutionary transition from facultative symbiosis to obligate mutualism facilitated by lateral gene transfer in an endosymbiont lineage.

    DOI: 10.1073/pnas.1409284111

  • Fine-scale geographical origin of an insect pest invading North America Reviewed

    Takahiro Hosokawa, Naruo Nikoh, Takema Fukatsu

    PloS one   9 ( 2 )   2014.2

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    Invasive species may rapidly spread throughout new areas once introduced, which may potentially lead to serious damage to local fauna and flora. Information on geographical origins, introduction routes, and biology in native regions of such invasive species is of critical importance in identifying means of transport, preventing reintroduction, and establishing control/eradication methods. The plataspid stinkbug Megacopta cribraria, known as kudzu bug, recently invaded North America and now has become not only an agricultural pest of soybean but also a nuisance pest. Here we investigate the geographical origin of the invasive M. cribraria populations. Phylogeographical analyses based on 8.7 kb mitochondrial DNA sequences of the introduced and East Asian native Megacopta populations identified a well-supported clade consisting of the introduced populations and M. punctatissima populations in the Kyushu region of Japan, which strongly suggests that the invading M. cribraria populations are derived from a M. punctatissima population in the Kyushu region. Therefore, the region is proposed as a promising source of natural enemies for biological control of the invasive pest. Based on the phylogenetic information, relationship and treatment of the two Megacopta species are discussed.

    DOI: 10.1371/journal.pone.0089107

  • Bacterial symbionts of a devastating coffee plant pest, the stinkbug Antestiopsis thunbergii (Hemiptera Pentatomidae) Reviewed

    Yu Matsuura, Takahiro Hosokawa, Mario Serracin, Genet M. Tulgetske, Thomas A. Miller, Takema Fukatsu

    Applied and environmental microbiology   80 ( 12 )   3769 - 3775   2014

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    Stinkbugs of the genus Antestiopsis, so-called antestia bugs or variegated coffee bugs, are notorious pests of coffee plants in Africa. We investigated the symbiotic bacteria associated with Antestiopsis thunbergii, a major coffee plant pest in Rwanda. PCR, cloning, sequencing, and phylogenetic analysis of bacterial genes identified four distinct bacterial lineages associated with A. thunbergii: A gammaproteobacterial gut symbiont and symbionts representing the genera Sodalis, Spiroplasma, and Rickettsia. In situ hybridization showed that the gut symbiont densely occupied the lumen of midgut crypts, whereas the Sodalis symbiont, the Spiroplasma symbiont, and the Rickettsia symbiont sparsely and sporadically infected various cells and tissues. Diagnostic PCR survey of 154 A. thunbergii individuals collected at 8 localities in Rwanda revealed high infection frequencies (100% for the gut symbiont, 51.3% for the Sodalis symbiont, 52.6% for the Spiroplasma symbiont, and 24.0% for the Rickettsia symbiont). These results suggest that the gut symbiont is the primary symbiotic associate of obligate nature for A. thunbergii, whereas the Sodalis symbiont, the Spiroplasma symbiont, and the Rickettsia symbiont are the secondary symbiotic associates of facultative nature. We observed high coinfection frequencies, i.e., 7.8% of individuals with quadruple infection with all the symbionts, 32.5% with triple infections with the gut symbiont and two of the secondary symbionts, and 39.6% with double infections with the gut symbiont and any of the three secondary symbionts, which were statistically not different from the expected coinfection frequencies and probably reflected random associations. The knowledge of symbiotic microbiota in A. thunbergii will provide useful background information for controlling this devastating coffee plant pest.

    DOI: 10.1128/AEM.00554-14

  • Diverse Strategies for Vertical Symbiont Transmission among Subsocial Stinkbugs Reviewed

    Takahiro Hosokawa, Mantaro Hironaka, Koichi Inadomi, Hiromi Mukai, Naruo Nikoh, Takema Fukatsu

    PloS one   8 ( 5 )   2013.5

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    Sociality may affect symbiosis and vice versa. Many plant-sucking stinkbugs harbor mutualistic bacterial symbionts in the midgut. In the superfamily Pentatomoidea, adult females excrete symbiont-containing materials from the anus, which their offspring ingest orally and establish vertical symbiont transmission. In many stinkbug families whose members are mostly non-social, females excrete symbiont-containing materials onto/beside eggs upon oviposition. However, exceptional cases have been reported from two subsocial species representing the closely related families Cydnidae and Parastrachiidae, wherein females remain nearby eggs for maternal care after oviposition, and provide their offspring with symbiont-containing secretions at later stages, either just before or after hatching. These observations suggested that sociality of the host stinkbugs may be correlated with their symbiont transmission strategies. However, we found that cydnid stinkbugs of the genus Adomerus, which are associated with gammaproteobacterial gut symbionts and exhibit elaborate maternal care over their offspring, smear symbiont-containing secretions onto eggs upon oviposition as many non-social stinkbugs do. Surface sterilization of the eggs resulted in aposymbiotic insects of slower growth, smaller size and abnormal body coloration, indicating vertical symbiont transmission via egg surface contamination and presumable beneficial nature of the symbiosis. The Adomerus symbionts exhibited AT-biased nucleotide compositions, accelerated molecular evolutionary rates and reduced genome size, while these degenerative genomic traits were less severe than those in the symbiont of a subsocial parastrachiid. These results suggest that not only sociality but also other ecological and evolutionary aspects of the host stinkbugs, including the host-symbiont co-evolutionary history, may have substantially affected their symbiont transmission strategies. (250 words).

    DOI: 10.1371/journal.pone.0065081

  • Comparative transcriptomics of the bacteriome and the spermalege of the bedbug Cimex lectularius (Hemiptera Cimicidae) Reviewed

    Minoru Moriyama, Ryuichi Koga, Takahiro Hosokawa, Naruo Nikoh, Ryo Futahashi, Takema Fukatsu

    Applied Entomology and Zoology   47 ( 3 )   233 - 243   2012.8

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    The bedbug Cimex lectularius is notorious as a blood-feeding exoparasite of human and other warm-blooded animals. In addition to its medical and hygienic importance, C. lectularius is known for its unique biological traits, including obligate nutritional mutualism with a vitamin-provisioning Wolbachia endosymbiont and a peculiar mating habit called traumatic insemination wherein male sperm is injected into the female body cavity, migrates to the ovary, and fertilizes eggs therein. For these unique traits, novel insect organs, the bacteriome for endosymbiosis and the spermalege for traumatic insemination, have evolved in the lineage of bedbugs. We constructed cDNA libraries of the bacteriome and the spermalege of C. lectularius, and performed expressed sequence tag (EST) analyses of these peculiar insect organs. In total 4480 ESTs were compiled, which were assembled into 2989 unique sequences (USs). The following ESTs and USs were identified from the different organs: 1151 ESTs and 901 USs from the female whole body; 1098 ESTs and 879 USs from the female bacteriome; 1145 ESTs and 783 USs from the male bacteriome; and 1086 ESTs and 920 USs from the female spermalege. These EST data will provide a valuable genetic resource for understanding the developmental and evolutionary aspects of these novel insect organs.

    DOI: 10.1007/s13355-012-0112-z

  • Polyphyly of gut symbionts in stinkbugs of the family cydnidae Reviewed

    Takahiro Hosokawa, Yoshitomo Kikuchi, Naruo Nikoh, Takema Fukatsu

    Applied and environmental microbiology   78 ( 13 )   4758 - 4761   2012.7

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    Symbiotic bacteria associated with midgut crypts of stinkbugs of the family Cydnidae, representing seven species and 13 populations, were investigated. All of the symbionts were species specific, and constituted at least four distinct lineages in the Gammaproteobacteria, indicating multiple evolutionary origins of the gut symbionts among the burrower bugs.

    DOI: 10.1128/AEM.00867-12

  • Symbiont-mediated insecticide resistance Reviewed

    Yoshitomo Kikuchi, Masahito Hayatsu, Takahiro Hosokawa, Atsushi Nagayama, Kanako Tago, Takema Fukatsu

    Proceedings of the National Academy of Sciences of the United States of America   109 ( 22 )   8618 - 8622   2012.5

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    Development of insecticide resistance has been a serious concern worldwide, whose mechanisms have been attributed to evolutionary changes in pest insect genomes such as alteration of drug target sites, up-regulation of degrading enzymes, and enhancement of drug excretion. Here, we report a previously unknown mechanism of insecticide resistance: Infection with an insecticide-degrading bacterial symbiont immediately establishes insecticide resistance in pest insects. The bean bug Riptortus pedestris and allied stinkbugs harbor mutualistic gut symbiotic bacteria of the genus Burkholderia, which are acquired by nymphal insects from environmental soil every generation. In agricultural fields, fenitrothion-degrading Burkolderia strains are present at very low densities. We demonstrated that the fenitrothion-degrading Burkholderia strains establish a specific and beneficial symbiosis with the stinkbugs and confer a resistance of the host insects against fenitrothion. Experimental applications of fenitrothion to field soils drastically enriched fenitrothion-degrading bacteria from undetectable levels to >80% of total culturable bacterial counts in the field soils, and >90% of stinkbugs reared with the enriched soil established symbiosis with fenitrothion-degrading Burkholderia. In a Japanese island where fenitrothion has been constantly applied to sugarcane fields, we identified a stinkbug population wherein the insects live on sugarcane and ≈8% of them host fenitrothion-degrading Burkholderia. Our finding suggests the possibility that the symbiont-mediated insecticide resistancemay develop even in the absence of pest insects, quickly establish within a single insect generation, and potentially move around horizontally between different pest insects and other organisms.

    DOI: 10.1073/pnas.1200231109

  • Reductive genome evolution, host-symbiont co-speciation and uterine transmission of endosymbiotic bacteria in bat flies Reviewed

    Takahiro Hosokawa, Naruo Nikoh, Ryuichi Koga, Masahiko Satô, Masahiko Tanahashi, Xian Ying Meng, Takema Fukatsu

    ISME Journal   6 ( 3 )   577 - 587   2012.3

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    Bat flies of the family Nycteribiidae are known for their extreme morphological and physiological traits specialized for ectoparasitic blood-feeding lifestyle on bats, including lack of wings, reduced head and eyes, adenotrophic viviparity with a highly developed uterus and milk glands, as well as association with endosymbiotic bacteria. We investigated Japanese nycteribiid bat flies representing 4 genera, 8 species and 27 populations for their bacterial endosymbionts. From all the nycteribiid species examined, a distinct clade of gammaproteobacteria was consistently detected, which was allied to endosymbionts of other insects such as Riesia spp. of primate lice and Arsenophonus spp. of diverse insects. In adult insects, the endosymbiont was localized in specific bacteriocytes in the abdomen, suggesting an intimate host-symbiont association. In adult females, the endosymbiont was also found in the cavity of milk gland tubules, which suggests uterine vertical transmission of the endosymbiont to larvae through milk gland secretion. In adult females of Penicillidia jenynsii, we discovered a previously unknown type of symbiotic organ in the Nycteribiidae: a pair of large bacteriomes located inside the swellings on the fifth abdominal ventral plate. The endosymbiont genes consistently exhibited adenine/thymine biased nucleotide compositions and accelerated rates of molecular evolution. The endosymbiont genome was estimated to be highly reduced, ∼0.76 Mb in size. The endosymbiont phylogeny perfectly mirrored the host insect phylogeny, indicating strict vertical transmission and host-symbiont co-speciation in the evolutionary course of the Nycteribiidae. The designation Candidatus Aschnera chinzeii is proposed for the endosymbiont clade.

    DOI: 10.1038/ismej.2011.125

  • Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs Reviewed

    Yu Matsuura, Yoshitomo Kikuchi, Takahiro Hosokawa, Ryuichi Koga, Xian Ying Meng, Yoichi Kamagata, Naruo Nikoh, Takema Fukatsu

    ISME Journal   6 ( 2 )   397 - 409   2012.2

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    We investigated seed bugs of the genus Nysius (Insecta: Hemiptera: Lygaeidae) for their symbiotic bacteria. From all the samples representing 4 species, 18 populations and 281 individuals, specific bacterial 16S rRNA gene sequences were consistently identified, which formed a distinct clade in the Gammaproteobacteria. In situ hybridization showed that the bacterium was endocellularly localized in a pair of large bacteriomes that were amorphous in shape, deep red in color, and in association with gonads. In the ovary of adult females, the endosymbiont was also localized in the 'infection zone' in the middle of each germarium and in the 'symbiont ball' at the anterior pole of each oocyte, indicating vertical transmission of the endosymbiont through the ovarial passage. Phylogenetic analyses based on bacterial 16S rRNA, groEL and gyrB genes consistently supported a coherent monophyly of the Nysius endosymbionts. The possibility of a sister relationship to 'Candidatus Kleidoceria schneideri', the bacteriome-associated endosymbiont of a lygaeid bug Kleidocerys resedae, was statistically rejected, indicating independent evolutionary origins of the endosymbionts in the Lygaeidae. The endosymbiont genes consistently exhibited AT-biased nucleotide compositions and accelerated rates of molecular evolution, and the endosymbiont genome was only 0.6 Mb in size. The endosymbiont phylogeny was congruent with the host insect phylogeny, suggesting strict vertical transmission and host-symbiont co-speciation over evolutionary time. Based on these results, we discuss the evolution of bacteriomes and endosymbionts in the Heteroptera, most members of which are associated with gut symbiotic bacteria. The designation Candidatus Schneideria nysicola is proposed for the endosymbiont clade.

    DOI: 10.1038/ismej.2011.103

  • Gut symbiotic bacteria in the cabbage bugs Eurydema rugosa and Eurydema dominulus (Heteroptera Pentatomidae) Reviewed

    Yoshitomo Kikuchi, Takahiro Hosokawa, Naruo Nikoh, Takema Fukatsu

    Applied Entomology and Zoology   47 ( 1 )   1 - 8   2012.2

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    The cabbage bugs Eurydema rugosa Motschulsky and Eurydema dominulus (Scopoli) (Heteroptera: Pentatomidae: Strachiini) possess a number of crypts in a posterior region of the midgut, which are filled with bacterial symbiont cells. Here we characterized the gut symbionts of Eurydema stinkbugs using molecular phylogenetic and histological techniques. Specific gammaproteobacteria were consistently identified from the posterior midgut of E. rugosa representing nine populations and E. dominulus representing six populations, respectively. The bacterial 16S rRNA gene sequences were identical within the species but slightly different (98. 2% sequence identity) between the species. Molecular phylogenetic analysis revealed that the Eurydema symbionts formed a well-defined monophyletic group in the Gammaproteobacteria. The symbionts were phylogenetically distinct from the gut symbionts of the stinkbug families Acanthosomatidae, Plataspidae, Parastrachiidae, Scutelleridae, and other pentatomid species, suggesting multiple evolutionary origins of the gut symbiotic bacteria among diverse stinkbugs. In situ hybridization confirmed that the symbiont is located in the cavity of the midgut crypts. Aposymbiotic insects of E. rugosa, which were produced by egg surface sterilization, were viable but suffered retarded growth, reduced body weight, and abnormal body color, suggesting the biological importance of the symbiont for the host.

    DOI: 10.1007/s13355-011-0081-7

  • Mothers never miss the moment A fine-tuned mechanism for vertical symbiont transmission in a subsocial insect Reviewed

    Takahiro Hosokawa, Mantaro Hironaka, Hiromi Mukai, Koichi Inadomi, Nobuhiko Suzuki, Takema Fukatsu

    Animal Behaviour   83 ( 1 )   293 - 300   2012.1

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    In a subsocial stinkbug Parastrachia japonensis, mature adult females lay both fertile eggs and trophic eggs in an underground nest, guard the egg mass for 15-20. days, and collect and provide food fruits for the nymphs. We investigated the vertical transmission of this species' obligate gut symbiont '. Candidatus Benitsuchiphilus tojoi' from mother to offspring. We observed that the mothers started to excrete a copious amount of symbiont-containing white mucus from the anus onto the egg mass at around 45. min before egg hatching; the excretion continued for approximately 40. min, and about 5. min later, fertile eggs in the egg mass started to hatch synchronously. The newborn nymphs immediately ingested the mucous secretion and the trophic eggs, which were completely consumed within 24. h. Mother removal and anal-sealing experiments confirmed that vertical symbiont transmission was mediated by the nymphs' exploitation of the mother-derived mucous secretion. Mother removal also resulted in asynchronous egg hatching, suggesting maternal involvement in the egg-hatching synchrony. These results indicate that vertical symbiont transmission in P. japonensis is finely tuned to the timing of egg hatching through intricate mother-offspring behavioural interactions, and highlight how sociality can evolutionarily affect symbiosis and vice versa.

    DOI: 10.1016/j.anbehav.2011.11.006

  • Reductive evolution of bacterial genome in insect gut environment Reviewed

    Naruo Nikoh, Takahiro Hosokawa, Kenshiro Oshima, Masahira Hattori, Takema Fukatsu

    Genome Biology and Evolution   3 ( 1 )   702 - 714   2011.12

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    Obligate endocellular symbiotic bacteria of insects and other organisms generally exhibit drastic genome reduction. Recently, it was shown that symbiotic gut bacteria of some stinkbugs also have remarkably reduced genomes. Here, we report the complete genome sequence of such a gut bacterium Ishikawaella capsulata of the plataspid stinkbug Megacopta punctatissima. Gene repertoire and evolutionary patterns, including AT richness and elevated evolutionary rate, of the 745,590 bp genome were strikingly similar to those of obligate c-proteobacterial endocellular insect symbionts like Buchnera in aphids and Wigglesworthia in tsetse flies. Ishikawaella was suggested to supply essential amino acids for the plant-sucking stinkbug as Buchnera does for the host aphid. Although Buchnera is phylogenetically closer to Wigglesworthia than to Ishikawaella, in terms of gene repertoire Buchnera was similar to Ishikawaella rather than to Wigglesworthia, providing a possible case of genome-level convergence of gene content. Meanwhile, several notable differences were identified between the genomes of Ishikawaella and Buchnera, including retention of TCA cycle genes and lack of flagellum-related genes in Ishikawaella, which may reflect their adaptation to distinct symbiotic habitats. Unexpectedly, Ishikawaella retained fewer genes related to cell wall synthesis and lipid metabolism than many endocellular insect symbionts. The plasmid of Ishikawaella encoded genes for arginine metabolism and oxalate detoxification, suggesting the possibility of additional Ishikawaella roles similar to those of human gut bacteria. Our data highlight strikingly similar evolutionary patterns that are shared between the extracellular and endocellular insect symbiont genomes.

    DOI: 10.1093/gbe/evr064

  • Obligate association with gut bacterial symbiont in Japanese populations of the southern green stinkbug Nezara viridula (Heteroptera Pentatomidae) Reviewed

    Akiyo Tada, Yoshitomo Kikuchi, Takahiro Hosokawa, Dmitry L. Musolin, Kenji Fujisaki, Takema Fukatsu

    Applied Entomology and Zoology   46 ( 4 )   483 - 488   2011.11

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    The southern green stinkbug Nezara viridula (Linnaeus) has a number of sac-like outgrowths, called crypts, in a posterior section of the midgut, wherein a specific bacterial symbiont is harbored. In previous studies on N. viridula from Hawaiian populations, experimental elimination of the symbiont caused few fitness defects in the host insect. Here we report that N. viridula from Japanese populations consistently harbors the same gammaproteobacterial gut symbiont, but, in contrast with previous work, experimental sterilization of the symbiont resulted in severe nymphal mortality, indicating an obligate host-symbiont relationship. Considering worldwide host-symbiont association and these experimental data, we suggest that N. viridula is generally and obligatorily associated with the gut symbiont, but that the effect of the symbiont on host biology may be different among geographic populations. Possible environmental factors that may affect the host-symbiont relationship are discussed.

    DOI: 10.1007/s13355-011-0066-6

  • Specific developmental window for establishment of an insect-microbe gut symbiosis Reviewed

    Yoshitomo Kikuchi, Takahiro Hosokawa, Takema Fukatsu

    Applied and environmental microbiology   77 ( 12 )   4075 - 4081   2011.6

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    The alydid stinkbug Riptortus pedestris is specifically associated with a beneficial Burkholderia symbiont in the midgut crypts. Exceptional among insect-microbe mutualistic associations, the Burkholderia symbiont is not vertically transmitted but orally acquired by nymphal insects from the environment every generation. Here we experimentally investigated the process of symbiont acquisition during the nymphal development of R. pedestris. In a field population, many 2nd instar nymphs were Burkholderia free, while all 3rd, 4th, and 5th instar nymphs were infected. When reared on soil-grown potted soybean plants, Burkholderia acquisition occurred at a drastically higher frequency in the 2nd instar than in the other instars. Oral administration of cultured Burkholderia cells showed that 2nd and 3rd instar nymphs are significantly more susceptible to the symbiont infection than 1st, 4th, and 5th instar nymphs. Histological observations revealed rudimentary midgut crypts in the 1st instar, in contrast to well-developed midgut crypts in the 2nd and later instars. These results indicate that R. pedestris acquires the Burkholderia symbiont from the environment mainly during the 2nd instar period and strongly suggest that the competence for the symbiont infection is developmentally regulated by the host side. Potential mechanisms involved in infection competence and possible reasons why the infection preferentially occurs in the 2nd instar are discussed.

    DOI: 10.1128/AEM.00358-11

  • Trophic eggs compensate for poor offspring feeding capacity in a subsocial burrower bug Reviewed

    Narumi Baba, Mantaro Hironaka, Takahiro Hosokawa, Hiromi Mukai, Shintaro Nomakuchi, Takatoshi Ueno

    Biology Letters   7 ( 2 )   194 - 196   2011.4

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    Various animals produce inviable eggs or egg-like structures called trophic eggs, which are presumed to be an extended maternal investment for the offspring. However, there is little knowledge about the ecological or physiological constraints associated with their evolutionary origin. Trophic eggs of the seminivorous subsocial burrower bug (Canthophorus niveimarginatus) have some unique characteristics. Trophic eggs are obligate for nymphal survival, and firstinstar nymphs die without them. To identify the cause of nymphal death, we hypothesized that first-instar nymphs starve to death because they cannot feed on anything but trophic eggs. Although first-instar nymphs fed on artificially exposed endosperm did survive, nymphs that were provided with intact seed were not able to penetrate the seed vessel and starved to death. Another hypothesis that trophic eggs play a role in transferring the midgut symbiont, essential for survival in heteropteran bugs, from mother to offspring was rejected because almost all nymphs had retained the symbiont without feeding on trophic eggs. These results suggest that poor feeding capacity of the offspring is the cause of nymphal death, and the important constraint that promotes the evolution of the curious trophic egg system in C. niveimarginatus.

    DOI: 10.1098/rsbl.2010.0707

  • An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts Reviewed

    Yoshitomo Kikuchi, Takahiro Hosokawa, Takema Fukatsu

    ISME Journal   5 ( 3 )   446 - 460   2011.3

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    Here, we investigated 124 stinkbug species representing 20 families and 5 superfamilies for their Burkholderia gut symbionts, of which 39 species representing 6 families of the superfamilies Lygaeoidea and Coreoidea were Burkholderia-positive. Diagnostic PCR surveys revealed high frequencies of Burkholderia infection in natural populations of the stinkbugs, and substantial absence of vertical transmission of Burkholderia infection to their eggs. In situ hybridization confirmed localization of the Burkholderia in their midgut crypts. In the lygaeoid and coreoid stinkbugs, development of midgut crypts in their alimentary tract was coincident with the Burkholderia infection, suggesting that the specialized morphological configuration is pivotal for establishment and maintenance of the symbiotic association. The Burkholderia symbionts were easily isolated as pure culture on standard microbiological media, indicating the ability of the gut symbionts to survive outside the host insects. Molecular phylogenetic analysis showed that the gut symbionts of the lygaeoid and coreoid stinkbugs belong to a β-proteobacterial clade together with Burkholderia isolates from soil environments and Burkholderia species that induce plant galls. On the phylogeny, the stinkbug-associated, environmental and gall-forming Burkholderia strains did not form coherent groups, indicating host-symbiont promiscuity among these stinkbugs. Symbiont culturing revealed that slightly different Burkholderia genotypes often coexist in the same insects, which is also suggestive of host-symbiont promiscuity. All these results strongly suggest an ancient but promiscuous host-symbiont relationship between the lygaeoid/coreoid stinkbugs and the Burkholderia gut symbionts. Possible mechanisms as to how the environmentally transmitted promiscuous symbiotic association has been stably maintained in the evolutionary course are discussed.

    DOI: 10.1038/ismej.2010.150

  • Bacterial symbionts of the giant jewel stinkbug Eucorysses grandis (Hemiptera Scutelleridae) Reviewed

    Nahomi Kaiwa, Takahiro Hosokawa, Yoshitomo Kikuchi, Naruo Nikoh, Xian Ying Meng, Nobutada Kimura, Motomi Ito, Takema Fukatsu

    Zoological science   28 ( 3 )   169 - 174   2011.3

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    Microbiological characterization of gut symbiotic bacteria in a limited number of stinkbugs of the families Acanthosomatidae, Plataspidae, Pentatomidae, Scutelleridae, Parastrachiidae, Alydidae and Pyrrhocoridae has shown symbiotic association with midgut bacteria to be common in phytophagous taxa of these heteropteran insects. Here we investigated the midgut bacterial symbiont of Eucorysses grandis, a stinkbug of the family Scutelleridae. A specific gammaproteobacterium was consistently identified in insects from five different geographic origins. The bacterium was detected in 64 of 64 insects sampled from three host populations. Phylogenetic analyses revealed that the bacterium constitutes a distinct lineage in the Gammaproteobacteria, neither closely related to the gut symbiont of another scutellerid stinkbug, Cantao ocellatus, nor to gut symbionts of other stinkbugs. Diagnostic PCR, in situ hybridization and electron microscopy demonstrated that the bacterium is located extracelluarly, in the midgut fourth section, which possesses crypts. These results indicate that the primary gut symbionts have multiple evolutionary origins in the Scutelleridae. A Sodalis-allied facultative symbiont was also identified in some insects from natural populations. Biological aspects of the primary gut symbiont and the secondary Sodalis-allied symbiont are discussed.

    DOI: 10.2108/zsj.28.169

  • Biological role of Nardonella endosymbiont in its weevil host Reviewed

    Takashi Kuriwada, Takahiro Hosokawa, Norikuni Kumano, Keiko Shiromoto, Dai Haraguchi, Takema Fukatsu

    PloS one   5 ( 10 )   2010.11

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    Weevils constitute the most species-rich animal group with over 60,000 described species, many of which possess specialized symbiotic organs and harbor bacterial endosymbionts. Among the diverse microbial associates of weevils, Nardonella spp. represent the most ancient and widespread endosymbiont lineage, having co-speciated with the host weevils for over 125 million years. Thus far, however, no empirical work on the role of Nardonella for weevil biology has been reported. Here we investigated the biological role of the Nardonella endosymbiont for the West Indian sweet potato weevil, Euscepes postfasciatus. This insect is an experimentally tractable pest insect that can easily be reared on a natural diet of sweet potato root as well as on an agar-based artificial diet. By larval feeding on an antibiotic-containing artificial diet, Nardonella infection was effectively eliminated from the treated insects. The antibiotic-treated insects exhibited significantly lighter body weight and lower growth rate than the control insects. Then, the antibiotic-treated insects and the control insects were respectively allowed to mate and oviposit on fresh sweet potatoes without the antibiotic. The offspring of the antibiotic-treated insects, which were all Nardonella-negative, exhibited significantly lighter body weight, smaller body size, lower growth rate and paler body color in comparison with the offspring of the control insects, which were all Nardonellapositive. In conclusion, the Nardonella endosymbiont is involved in normal growth and development of the host weevil. The biological role of the endosymbiont probably underlies the long-lasting host-symbiont co-speciation in the evolutionary course of weevils.

    DOI: 10.1371/journal.pone.0013101

  • Phylogenetic position and peculiar genetic traits of a midgut bacterial symbiont of the stinkbug parastrachia japonensis Reviewed

    Takahiro Hosokawa, Yoshitomo Kikuchi, Naruo Nikon, Xian Ying Meng, Mantaro Hironaka, Takema Fukatsu

    Applied and environmental microbiology   76 ( 13 )   4130 - 4135   2010.7

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    The stinkbug Parastrachia japonensis (Hemiptera: Parastrachiidae) is known for its prolonged prereproductive nonfeeding period, maternal care of eggs in an underground nest, and maternal collection and provisioning of food (fruits) for nymphs. A previous study suggested that a bacterial symbiont is involved in uric acid recycling in this insect during the nonfeeding period, but the identity of this symbiont has not been determined. Here we characterized a novel bacterial symbiont obtained from P. japonensis. Molecular phylogenetic analyses based on 16S rRNA, gyrB, and groEL gene sequences consistently indicated that this symbiont constituted a distinct lineage in the Gammaproteobacteria that has no close relatives but is allied with gut symbionts of acanthosomatid and plataspid stinkbugs, as well as with endocellular symbionts of sharpshooters, tsetse flies, and aphids. The symbiont genes had a remarkably AT-biased nucleotide composition and exhibited significantly accelerated molecular evolution. The symbiont genome was extremely reduced; its size was estimated to be 0.85 Mb. These results suggest that there has been an intimate host-symbiont association over evolutionary time. The symbiont was localized in swollen crypts in a posterior part of the midgut, which was a specialized symbiotic organ. The possibility that the symbiont is involved in uric acid recycling is discussed. The designation "Candidatus Benitsuchiphilus tojoi" is proposed for the symbiont.

    DOI: 10.1128/AEM.00616-10

  • Primary gut symbiont and secondary, sodalis-allied symbiont of the scutellerid stinkbug cantao ocellatus Reviewed

    Nahomi Kaiwa, Takahiro Hosokawa, Yoshitomo Kikuchi, Naruo Nikoh, Xian Ying Meng, Nobutada Kimura, Motomi Ito, Takema Fukatsu

    Applied and Environmental Microbiology   76 ( 11 )   3486 - 3494   2010.6

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    Symbiotic associations with midgut bacteria have been commonly found in diverse phytophagous heteropteran groups, where microbiological characterization of the symbiotic bacteria has been restricted to the stinkbug families Acanthosomatidae, Plataspidae, Pentatomidae, Alydidae, and Pyrrhocoridae. Here we investigated the midgut bacterial symbiont of Cantao ocellatus, a stinkbug of the family Scutelleridae. A specific gammaproteobacterium was consistently identified from the insects of different geographic origins. The bacterium was detected in all 116 insects collected from 9 natural host populations. Phylogenetic analyses revealed that the bacterium constitutes a distinct lineage in the Gammaproteobacteria, not closely related to gut symbionts of other stinkbugs. Diagnostic PCR and in situ hybridization demonstrated that the bacterium is extracellularly located in the midgut 4th section with crypts. Electron microscopy of the crypts revealed a peculiar histological configuration at the host-symblont interface. Egg sterilization experiments confirmed that the bacterium is vertically transmitted to stinkbug nymphs via egg surface contamination. In addition to the gut symbiont, some individuals of C. ocellatus harbored another bacterial symbiont in their gonads, which was closely related to Sodalis glossinidius, the secondary endosymbiont of tsetse flies. Biological aspects of the primary gut symbiont and the secondary Sodalis-allied symbiont are discussed.

    DOI: 10.1128/AEM.00421-10

  • Nardonella endosymbiont in the West Indian sweet potato weevil Euscepes postfasciatus (Coleoptera Curculionidae) Reviewed

    Takahiro Hosokawa, Takema Fukatsu

    Applied Entomology and Zoology   45 ( 1 )   115 - 120   2010.3

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    The West Indian sweet potato weevil, Euscepes postfasciatus, is a notorious pest of the sweet potato, Ipomoea batatas. We examined the potential presence of a bacterial endosymbiont in the pest weevil. The bacterial 16S rRNA gene and groEL gene were detected by PCR from the insects. Cloning, sequencing and molecular phylogenetic analyses of the bacterial genes demonstrated that E. postfasciatus is associated with a γ -proteobacterial endosymbiont of the genus Nardonella. In situ hybridization detected the endosymbiont in the female ovaries, indicating its transovarial transmission through host generations. This study is the first to identify Nardonella from the weevil subfamily Cryptorhynchinae. The potential relevance of the endosymbiont in the biology and management of E. postfasciatus is discussed.

    DOI: 10.1303/aez.2010.115

  • Wolbachia as a bacteriocyte-associated nutritional mutualist Reviewed

    Takahiro Hosokawa, Ryuichi Koga, Yoshitomo Kikuchi, Xian Ying Meng, Takema Fukatsu

    Proceedings of the National Academy of Sciences of the United States of America   107 ( 2 )   769 - 774   2010.2

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    Many insects are dependent on bacterial symbionts that provide essential nutrients (ex. aphid-Buchnera and tsetse-Wiglesworthia associations), wherein the symbionts are harbored in specific cells called bacteriocytes that constitute a symbiotic organ bacteriome. Facultative and parasitic bacterial symbionts like Wolbachia have been regarded as evolutionarily distinct from such obligate nutritional mutualists. However, we discovered that, in the bedbug Cimex lectularius, Wolbachia resides in a bacteriome and appears to be an obligate nutritional mutualist. Two bacterial symbionts, a Wolbachia strain and an unnamed γ-proteobacterium, were identified from different strains of the bedbug. The Wolbachia symbiont was detected fromall of the insects examined whereas the γ-proteobacterium was found in a part of them. The Wolbachia symbiont was specifically localized in the bacteriomes and vertically transmitted via the somatic stemcell niche of germalia to oocytes, infecting the incipient symbiotic organ at an early stage of the embryogenesis. Elimination of the Wolbachia symbiont resulted in retarded growth and sterility of the host insect. These deficiencies were rescued by oral supplementation of B vitamins, confirming the essential nutritional role of the symbiont for the host. The estimated genome size of the Wolbachia symbiont was around 1.3 Mb, which was almost equivalent to the genome sizes of parasitic Wolbachia strains of other insects. These results indicate that bacteriocyte-associated nutritional mutualism can evolve from facultative and prevalent microbial associates like Wolbachia, highlighting a previously unknown aspect of the parasitism-mutualism evolutionary continuum.

    DOI: 10.1073/pnas.0911476107

  • Candidatus Curculioniphilus buchneri,quot; a novel clade of bacterial endocellular symbionts from weevils of the genus Curculio Reviewed

    Hirokazu Toju, Takahiro Hosokawa, Ryuichi Koga, Naruo Nikoh, Xian Ying Meng, Nobutada Kimura, Takema Fukatsu

    Applied and environmental microbiology   76 ( 1 )   275 - 282   2010.1

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    Here we investigated the bacterial endosymbionts of weevils of the genus Curculio. From all four species of Curculio weevils examined, a novel group of bacterial gene sequences were consistently identified. Molecular phylogenetic analyses demonstrated that the sequences formed a distinct clade in the Gammaproteobacteria, which was not related to previously known groups of weevil endosymbionts such as Nardonella spp. and Sodalis-allied symbionts. In situ hybridization revealed that the bacterium was intracellularly harbored in a bacteriome associated with larval midgut. In adult females, the bacterium was localized in the germalia at the tip of each overiole, suggesting vertical transmission via ovarial passage. Diagnostic PCR surveys detected high prevalence of the bacterial infection in natural host populations. Electron microscopy identified the reduced cell wall of the bacterial cells, and the bacterial genes exhibited AT-biased nucleotide composition and accelerated molecular evolution, which are suggestive of a long-lasting endosymbiotic association. On the basis of these results, we conclude that the novel endocellular bacteria represent the primary symbiont of Curculio weevils and proposed the designation quot;Condidatus Curculioniphilus buchneri.quot; In addition to quot;Ca. CurcuIioniphilus,quot; we identified Sodalis-allied gammaproteobacterial endosymbionts from the chestnut weevil, Curculio sikkimensis, which exhibited partial infection frequencies in host insect populations and neither AT-biased nucleotide composition nor accelerated molecular evolution. We suggest that such Sodalis-allied secondary symbionts in weevils might provide a potential source for symbiont replacements, as has occurred in an ancestor of Sitophilus grain weevils.

    DOI: 10.1128/AEM.02154-09

  • Intestinal endocellular symbiotic bacterium of the macaque louse Pedicinus obtusus Distinct endosymbiont origins in anthropoid primate lice and the old world monkey louse Reviewed

    Takema Fukatsu, Takahiro Hosokawa, Ryuichi Koga, Naruo Nikoh, Takuya Kato, Shin Ichi Hayama, Haruo Takefushi, Ichirou Tanaka

    Applied and environmental microbiology   75 ( 11 )   3796 - 3799   2009.6

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    A symbiotic bacterium of the macaque louse, Pedicinus obtusus, was characterized. The symbiont constituted a gammaproteobacterial lineage distinct from the symbionts of anthropoid primate lice, localized in the midgut epithelium and the ovaries and exhibiting AT-biased genes and accelerated molecular evolution. The designation "Candidatus Puchtella pedicinophila" was proposed for it.

    DOI: 10.1128/AEM.00226-09

  • Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs Reviewed

    Yoshitomo Kikuchi, Takahiro Hosokawa, Naruo Nikoh, Xian Ying Meng, Yoichi Kamagata, Takema Fukatsu

    BMC Biology   7   2009.1

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    Background: Host-symbiont co-speciation and reductive genome evolution have been commonly observed among obligate endocellular insect symbionts, while such examples have rarely been identified among extracellular ones, the only case reported being from gut symbiotic bacteria of stinkbugs of the family Plataspidae. Considering that gut symbiotic communities are vulnerable to invasion of foreign microbes, gut symbiotic associations have been thought to be evolutionarily not stable. Stinkbugs of the family Acanthosomatidae harbor a bacterial symbiont in the midgut crypts, the lumen of which is completely sealed off from the midgut main tract, thereby retaining the symbiont in the isolated cryptic cavities. We investigated histological, ecological, phylogenetic, and genomic aspects of the unique gut symbiosis of the acanthosomatid stinkbugs. Results: Phylogenetic analyses showed that the acanthosomatid symbionts constitute a distinct clade in the γ-Proteobacteria, whose sister groups are the obligate endocellular symbionts of aphids Buchnera and the obligate gut symbionts of plataspid stinkbugs Ishikawaella. In addition to the midgut crypts, the symbionts were located in a pair of peculiar lubricating organs associated with the female ovipositor, by which the symbionts are vertically transmitted via egg surface contamination. The symbionts were detected not from ovaries but from deposited eggs, and surface sterilization of eggs resulted in symbiont-free hatchlings. The symbiont-free insects suffered retarded growth, high mortality, and abnormal morphology, suggesting important biological roles of the symbiont for the host insects. The symbiont phylogeny was generally concordant with the host phylogeny, indicating host-symbiont co-speciation over evolutionary time despite the extracellular association. Meanwhile, some local host-symbiont phylogenetic discrepancies were found, suggesting occasional horizontal symbiont transfers across the host lineages. The symbionts exhibited AT-biased nucleotide composition, accelerated molecular evolution, and reduced genome size, as has been observed in obligate endocellular insect symbionts. Conclusion: Comprehensive studies of the acanthosomatid bacterial symbiosis provide new insights into the genomic evolution of extracellular symbiotic bacteria: host-symbiont co-speciation and drastic genome reduction can occur not only in endocellular symbiotic associations but also in extracellular ones. We suggest that many more such cases might be discovered in future surveys.

    DOI: 10.1186/1741-7007-7-2

  • Symbiont acquisition alters behaviour of stinkbug nymphs Reviewed

    Takahiro Hosokawa, Yoshitomo Kikuchi, Masakazu Shimada, Takema Fukatsu

    Biology Letters   4 ( 1 )   45 - 48   2008.2

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    In parasitic associations, the evolutionary interest of a symbiont contradicts that of a host, which sometimes causes the phenomena so-called 'parasite manipulation' wherein symbiont infection alters host behaviour to facilitate its vertical/horizontal transmission. In mutualistic associations, meanwhile, symbiont-induced alteration of host behaviour that enhances its transmission has been little described. Here we report such a case in the stinkbug Megacopta punctatissima associated with an obligate gut bacterium. When female stinkbugs lay eggs, small particles called 'symbiont capsules' are deposited underside of the egg mass. Newborn nymphs immediately acquire the symbiont from the capsule, and then aggregate and become quiescent. By manipulating the levels of symbiont supply to newborn nymphs experimentally, we demonstrated that (i) experimental depletion of the symbiont resulted in the occurrence of wandering nymphs, (ii) the less symbiont supply, the more wandering nymphs, and (iii) almost all wandering nymphs were either symbiont-free or symbiont-depleted, whereas the majority of resting nymphs were infected with sufficient titres of the symbiont. These results strongly suggest that the nymphal behaviour is strongly influenced by the success/failure of the symbiont acquisition, thereby ensuring transmission of the essential symbiont and minimizing the energy and time spent for the activity.

    DOI: 10.1098/rsbl.2007.0510

  • Capsule-transmitted obligate gut bacterium of plataspid stinkbugs A novel model system for insect symbiosis studies

    Takema Fukatsu, Takahiro Hosokawa

    Insect Symbiosis   3   95 - 122   2008.1

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    Symbiotic microorganisms are universally found in the gut, body cavity, or cells of a wide variety of insects. Some obligate symbionts are of a mutualistic nature and contribute to the fitness of their hosts, whereas other facultative symbionts are rather parasitic and tend to cause negative effects on their hosts (Bourtzis and Miller, 2003, 2006).

    DOI: 10.1201/9781420064117

  • Diversity of bacterial symbiosis in stinkbugs

    Yoshitomo Kikuchi, Takahiro Hosokawa, Takema Fukatsu

    Microbial Ecology Research Trends   39 - 63   2008.1

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    Many animals and plants establish symbiotic associations with benevolent microorganisms. In particular, most of insects that feed exclusively on restricted diets, such as plant sap, vertebrate blood or woody material, usually possess symbiotic microorganisms inside their body. Recent studies have suggested that more than 50% of insect species may be benefited from such endosymbiotic partners. Among these insects, members of the Heteroptera, known as true bugs or stinkbugs, exhibit an extraordinary diversity in their microbial symbiotic system. Such diversity is exemplified by: (i) physiological impact of the symbiotic associations on the host fitness ranging from parasitic to mutualistic; (ii) interdependence of the symbiotic associations ranging from facultative to obligate; (iii) location of the symbiont ranging from extracellular in gut cavity to intracellular in specialized cells; (iv) among the extracellular associations, specialized symbiotic structures such as midgut sacs and tubular outgrowths, whose cavity harbors specific symbiotic bacteria, varying in their number and arrangement; and (v) mechanisms for symbiont transmission ranging from vertical to environmental. Here, the current biological knowledge of the diverse stinkbug-bacteria symbioses is reviewed, which will provide novel insights into and useful model systems for understanding of the host-symbiont interactions and evolution.

  • How many symbionts are provided by mothers, acquired by offspring, and needed for successful vertical transmission in an obligate insect-bacterium mutualism? Reviewed

    Takahiro Hosokawa, Yoshitomo Kikuchi, Takema Fukatsu

    Molecular Ecology   16 ( 24 )   5316 - 5325   2007.12

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    Vertical symbiont transmission is among the most pivotal processes for maintenance of symbiotic associations. However, it is poorly understood whether and how the levels of resource allocation and investment upon vertical transmission are regulated. The stinkbug Megacopta punctatissima is obligatorily associated with the gut symbiotic bacterium 'Candidatus Ishikawaella capsulata', whose transmission is mediated by a unique mechanism called 'symbiont capsule'. We investigated the population dynamics of the symbiont during vertical transmission in the host-symbiont mutualism. The stinkbug mothers produced one capsule for around 3.6 eggs irrespective of clutch size, suggesting a strict maternal control over symbiont supply for the offspring. However, experimental manipulation of egg/capsule ratios revealed that one capsule is sufficient for symbiont transmission to six nymphs. Quantitative polymerase chain reaction analyses demonstrated that a capsule contains 1.2 × 108 symbionts, a newborn nymph possesses 2 × 10 7 symbionts from a capsule, and thus one capsule certainly contains a sufficient amount of symbiont cells for six nymphs. These results indicated that the stinkbug mothers produce 1.7 times more symbiont capsules than needed. The newborn nymphs consistently harboured around 2 × 107 symbionts, also suggesting a nymphal control over symbiont transmission. The threshold symbiont titre minimally needed for successful vertical transmission was estimated to be 1.9 × 106 symbionts, which is only 1/10 of the actual symbiont titre detected in a newborn nymph. These results illuminate several ecological factors that may be relevant to parental and offspring controls over symbiotic resource allocation through host insect generations.

    DOI: 10.1111/j.1365-294X.2007.03592.x

  • Obligate symbiont involved in pest status of host insect Reviewed

    Takahiro Hosokawa, Yoshitomo Kikuchi, Masakazu Shimada, Takema Fukatsu

    Proceedings of the Royal Society B: Biological Sciences   274 ( 1621 )   1979 - 1984   2007.8

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    The origin of specific insect genotypes that enable efficient use of agricultural plants is an important subject not only in applied fields like pest control and management but also in basic disciplines like evolutionary biology. Conventionally, it has been presupposed that such pest-related ecological traits are attributed to genes encoded in the insect genomes. Here, however, we report that pest status of an insect is principally determined by symbiont genotype rather than by insect genotype. A pest stinkbug species, Megacopta punctatissima, performed well on crop legumes, while a closely related non-pest species, Megacopta cribraria, suffered low egg hatch rate on the plants. When their obligate gut symbiotic bacteria were experimentally exchanged between the species, their performance on the crop legumes was, strikingly, completely reversed: the pest species suffered low egg hatch rate, whereas the non-pest species restored normal egg hatch rate and showed good performance. The low egg hatch rates were attributed to nymphal mortality before or upon hatching, which were associated with the symbiont from the non-pest stinkbug irrespective of the host insect species. Our finding sheds new light on the evolutionary origin of insect pests, potentially leading to novel approaches to pest control and management.

    DOI: 10.1098/rspb.2007.0620

  • Insect-microbe mutualism without vertical transmission A stinkbug acquires a beneficial gut symbiont from the environment every generation Reviewed

    Yoshitomo Kikuchi, Takahiro Hosokawa, Takema Fukatsu

    Applied and environmental microbiology   73 ( 13 )   4308 - 4316   2007.7

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    The broad-headed bug Riptortus clavatus (Heteroptera: Alydidae) possesses a number of crypts at a posterior midgut region, which house a dense population of a bacterial symbiont belonging to the genus Burkholderia. Although the symbiont is highly prevalent (95 to 100%) in the host populations, the symbiont phylogeny did not reflect the host systematics at all. In order to understand the mechanisms underlying the promiscuous host-symbiont relationship despite the specific and prevalent association, we investigated the transmission mode and the fitness effects of the Burkholderia symbiont in R. clavatus. Inspection of eggs and a series of rearing experiments revealed that the symbiont is not vertically transmitted but is environmentally acquired by nymphal insects. The Burkholderia symbiont was present in the soil of the insect habitat, and a culture strain of the symbiont was successfully isolated from the insect midgut Rearing experiments by using sterilized soybean bottles demonstrated that the cultured symbiont is able to establish a normal and efficient infection in the host insect, and the symbiont infection significantly improves the host fitness. These results indicated that R. clavatus postnatally acquires symbiont of a beneficial nature from the environment every generation, uncovering a previously unknown pathway through which a highly specific insect-microbe association is maintained. We suggest that the stinkbug-Burkholderia relationship may be regarded as an insect analogue of the well-known symbioses between plants and soil-associated microbes, such as legume-Rhizobium and alder-Frankia relationships, and we discuss the evolutionary relevance of the mutualistic but promiscuous insect-microbe association.

    DOI: 10.1128/AEM.00067-07

  • Alternative mating strategy of small male Megacopta punctatissima (Hemiptera Plataspidae) in the presence of large intraspecific males Reviewed

    C. Himuro, Takahiro Hosokawa, N. Suzuki

    Annals of the Entomological Society of America   99 ( 5 )   974 - 977   2006.11

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    We investigated the influence of the presence of large males on the mating tactics of small males of the stink bug Megacopta punctatissima (Montandon) (Hemiptera: Plataspidae) by using laboratory experiments. In the presence of large males, the mating acceptance rate of females (the proportion of copulating males to the number of courting males) and the mating success (the proportion of copulating males to the total number of males) of large males were significantly higher than those of small males. Therefore, sexual selection favors larger male body size at mating. Although only 15.4% of small males courted females in the presence of large males, 57.5% of small males courted females in the absence of large males. Consequently, the mating success of small males was conspicuously higher in the absence of large males than in the presence of large males. We suggest that small males adopt an alternative mating strategy in which their courtship behavior is the same as that of large males, but their decision to court females depends on the presence or absence of large rival males.

    DOI: 10.1603/0013-8746(2006)99[974:AMSOSM]2.0.CO;2

  • Prevalence of a non-male-killing spiroplasma in natural populations of Drosophila hydei Reviewed

    Daisuke Kageyama, Hisashi Anbutsu, Masayoshi Watada, Takahiro Hosokawa, Masakazu Shimada, Takema Fukatsu

    Applied and Environmental Microbiology   72 ( 10 )   6667 - 6673   2006.10

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    Male-killing phenotypes are found in a variety of insects and are often associated with maternally inherited endosymbiotic bacteria. In several species of Drosophila, male-killing endosymbionts of the genus Spiroplasma have been found at low frequencies (0.1 to 3%). In this study, spiroplasma infection without causing male-killing was shown to be prevalent (23 to 66%) in Japanese populations of Drosophila hydei. Molecular phylogenetic analyses showed that D. hydei was infected with a single strain of spiroplasma, which was closely related to male-killing spiroplasmas from other Drosophila species. Artificial-transfer experiments suggested that the spiroplasma genotype rather than the host genotype was responsible for the absence of the male-killing phenotype. Infection densities of the spiroplasma in the natural host, D. hydei, and in the artificial host, Drosophila melanogaster, were significantly lower than those of the male-killing spiroplasma NSRO, which was in accordance with the hypothesis that a threshold infection density is needed for the spiroplasma-induced male-killing expression.

    DOI: 10.1128/AEM.00803-06

  • Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria Reviewed

    Takahiro Hosokawa, Yoshitomo Kikuchi, Naruo Nikoh, Masakazu Shimada, Takema Fukatsu

    PLoS Biology   4 ( 10 )   1841 - 1851   2006.10

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    Host-symbiont cospeciation and reductive genome evolution have been identified in obligate endocellular insect symbionts, but no such example has been identified from extracellular ones. Here we first report such a case in stinkbugs of the family Plataspidae, wherein a specific gut bacterium is vertically transmitted via "symbiont capsule." In all of the plataspid species, females produced symbiont capsules upon oviposition and their gut exhibited specialized traits for capsule production. Phylogenetic analysis showed that the plataspid symbionts constituted a distinct group in the γ-Proteobacteria, whose sister group was the aphid obligate endocellular symbionts Buchnera. Removal of the symbionts resulted in retarded growth, mortality, and sterility of the insects. The host phylogeny perfectly agreed with the symbiont phylogeny, indicating strict host-symbiont cospeciation despite the extracellular association. The symbionts exhibited AT-biased nucleotide composition, accelerated molecular evolution, and reduced genome size, as has been observed in obligate endocellular insect symbionts. These findings suggest that not the endocellular conditions themselves but the population genetic attributes of the vertically transmitted symbionts are probably responsible for the peculiar genetic traits of these insect symbionts. We proposed the designation "Candidatus Ishikawaella capsulata" for the plataspid symbionts. The plataspid stinkbugs, wherein the host-symbiont associations can be easily manipulated, provide a novel system that enables experimental approaches to previously untouched aspects of the insect-microbe mutualism. Furthermore, comparative analyses of the sister groups, the endocellular Buchnera and the extracellular Ishikawaella, would lead to insights into how the different symbiotic lifestyles have affected their genomic evolution.

    DOI: 10.1371/journal.pbio.0040337

  • The making of symbiont capsule in the plataspid stinkbug Megacopta punctatissima Reviewed

    Takahiro Hosokawa, Yoshitomo Kikuchi, Ying Meng Xien, Takema Fukatsu

    FEMS microbiology ecology   54 ( 3 )   471 - 477   2005.11

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    In stinkbugs of the family Plataspidae, adult females deposit small brownish particles, containing specific symbiotic bacteria inside, on the underside of their egg mass. Newborn nymphs ingest the content of the unique structure, called "symbiont capsule", whereby vertical transmission of the symbiont occurs. We investigated the fine structure and the formation process of the symbiont capsule in the Japanese common plataspid stinkbug, Megacopta punctatissima, by using light and electron microscopy. It was demonstrated that (i) the capsule consists of three structural components, namely "symbionts", "matrix" and "envelope"; (ii) the posterior midgut of adult females is characterized by several specific sections with peculiar anatomical traits, including "thin crypt-bearing midgut (TCM) section", "swollen crypt-bearing midgut (SCM) section" and "brownish enlarged midgut (BEM) end section"; (iii) the different capsule components, symbionts, matrix and envelope, are produced and/or supplied by the specialized midgut sections, TCM, SCM and BEM, respectively; and (iv) the capsule components are stored in BEM and excreted during oviposition to produce the symbiont capsules. These results strongly suggested that the host insect incurs a substantial cost for the symbiont transmission. Ecological and evolutionary implications of the highly developed, female-specific system for symbiont transmission were discussed.

    DOI: 10.1016/j.femsec.2005.06.002

  • Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, megacopta punctatissima Reviewed

    T. Fukatsu, Takahiro Hosokawa

    Applied and Environmental Microbiology   68 ( 1 )   389 - 396   2002.1

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    The Japanese common plataspid stinkbug, Megacopta punctatissima, deposits small brown particles, or symbiont capsules, on the underside of the egg mass for the purpose of transmission of symbiotic bacteria to the offspring. We investigated the microbiological aspects of the bacteria contained in the capsule, such as microbial diversity, phylogenetic placement, localization in vivo, and fitness effects on the host insect. Restriction fragment length polymorphism analysis of 16S ribosomal DNA clones revealed that a single bacterial species dominates the microbiota in the capsule. The bacterium was not detected in the eggs but in the capsules, which unequivocally demonstrated that the bacterium is transmitted to the offspring of the insect orally rather than transovarially, through probing of the capsule content. Molecular phylogenetic analysis showed that the bacterium belongs to the γ-subdivision of the Proteobacteria. In adult insects the bacterium was localized in the posterior section of the midgut. Deprivation of the bacterium from the nymphs resulted in retarded development, arrested growth, abnormal body coloration, and other symptoms, suggesting that the bacterium is essential for normal development and growth of the host insect.

    DOI: 10.1128/AEM.68.1.389-396.2002

  • Significance of prolonged copulation under the restriction of daily reproductive time in the stink bug Megacopta punctatissima (heteroptera plataspidae) Reviewed

    Takahiro Hosokawa, Nobuhiko Suzuki

    Annals of the Entomological Society of America   94 ( 5 )   750 - 754   2001.1

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    Copulation duration and daily reproductive activity pattern of the stink bug Megacopta punctatissima Montandon were investigated in the laboratory and the field. Mean copulation duration was >10 h regardless of sex ratio and few copulations continued for more than 24 h in the laboratory. In the field, mating aggregations and copulations were found from 1400 to 1000 hours on the next day, but bugs tended not to copulate from 1000 to 1400 hours. This daily reproductive activity pattern seemed to restrict the copulation duration to about 24 h at the longest. Sperm transfer from a male to a female spermatheca was complete within 2-4 h. Thus, it appears that copulations over 4 h serve as postcopulatory mate guarding. However, copulations did not always continue until pviposition because female oviposited after about a 7-d interval. Our findings suggest the possibility that prolonged copulations that do not continue until oviposition may also function as postcopulatory mate guarding within daily reproductive time. Alternative hypotheses, such as copulatory courship, for prolonged copulation of M. punctatissisma are also discussed.

    DOI: 10.1603/0013-8746(2001)094[0750:SOPCUT]2.0.CO;2

  • Mating aggregation and copulatory success by males of the stink bug, Megacopta punctatissima (Heteroptera Plataspidae) Reviewed

    Takahiro Hosokawa, Nobuhiko Suzuki

    Applied Entomology and Zoology   35 ( 1 )   93 - 99   2000.1

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    Language:English   Publishing type:Research paper (scientific journal)  

    In the stink bug, Megacopta punctatissima, which forms mating aggregations, male mating behaviors and the copulatory success of males were examined in experimental populations with 4 different sex ratios. In the male-biased sex ratio, more males tended to stay in "copulatory aggregations" including at least a mating pair rather than in "non-copulatory aggregations" including no mating pair, despite a scarcity of non-copulating females in such aggregations. However, when copulating females were included, there were more females in the copulatory aggregations than those in the non-copulatory aggregations. Therefore, the results appear to suggest that males also regarded copulating females as potential mates. Males which had immigrated to an aggregation showed a higher copulatory success than resident males in the aggregation at a male-biased sex ratio. Moreover, males showed a large variation in mating success, and those which had a higher mating success tended to stay in aggregations of female-biased sex ratios. These results suggest that females may choose their mates in mating aggregations, and that the choice may influence male mating success more acutely in a male-biased sex ratio.

    DOI: 10.1303/aez.2000.93

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Books

  • カメムシの母が子に伝える共生細菌-必須相利共生の多様性と進化-

    細川貴弘(Role:Sole author)

    共立出版  2017.11 

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    Language:Japanese   Book type:General book, introductory book for general audience

Presentations

  • チャバネアオカメムシの必須共生細菌の種内多型とその起源

    細川貴弘

    日本進化学会  2016.8 

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    Event date: 2018.5

    Language:Japanese   Presentation type:Symposium, workshop panel (public)  

    Country:Japan  

  • カメムシ上科における共生細菌の垂直伝播機構および共生細菌の置換実験

    細川貴弘

    日本応用動物昆虫学会  2018.3 

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    Event date: 2018.5

    Language:Japanese  

    Country:Japan  

  • 南西諸島のカメムシ類における必須共生細菌の種内多型はどのようにして生じたか

    細川 貴弘, 石井佳子, 深津武馬

    日本進化学会  2015.8 

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    Event date: 2015.8

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:中央大学 後楽園キャンパス   Country:Japan  

    成長や繁殖に必須な共生微生物を体内に保持し、垂直伝播によって維持している昆虫は多い。このような共生系では宿主昆虫と共生微生物の共種分化と共進化によって、各宿主に種特異的な共生微生物が進化しているのが一般的である。ところが我々は、南西諸島に生息するチャバネアオカメムシの必須共生細菌には著しい種内多型が存在するという前代未聞の現象を発見した。この共生細菌多型の形成過程を解明するために大規模な野外サンプリング、分子系統解析、飼育実験をおこなったところ、チャバネアオカメムシの必須共生細菌と同等の生物機能をもった自

  • チャバネアオカメムシの必須共生細菌の多型はいかにして生じたか?

    細川 貴弘, 石井佳子, 深津武馬

    日本生態学会  2015.3 

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    Event date: 2015.3

    Language:Japanese   Presentation type:Oral presentation (general)  

    Country:Japan  

    成長や繁殖に必須な共生微生物を体内に保持し、親から子への垂直伝播によって維持している昆虫は多い。このような共生系においては、宿主昆虫と共生微生物の間の共種分化と共進化によって各宿主に種特異的な共生微生物が進化しているのが一般的である。ところが我々はチャバネアオカメムシの必須共生細菌には著しい種内多型が存在するという前代未聞の現象を発見した。本講演ではこの共生細菌多型の形成過程と維持機構を解明するためにおこなった一連の飼育実験について報告する。まず、これまでに見つかっている6タイプの共生細菌の生物的機能に違いがあるかどうかを明らかにするために共生細菌の相互入れ換え実験をおこなったところ、共生細菌を入れ換えたカメムシも正常に成長・繁殖した。したがって6タイプの共生細菌は同等の生物的機能を持つと考えられた。次に、共生細菌に近縁なPantoea属の自由生活細菌(土壌から単離されたP. dispersaとヒトの傷口から単離されたP. agglomerans)をそれぞれカメムシと共生させたところ、驚くべきことに宿主カメムシは正常に成長・繁殖した。この結果は、外環境中に生息するPantoea属の自由生活細菌の一部もカメムシの共生細菌と同等の生物的機能を持つことを示している。カメムシの生息地の土壌細菌群集の解析から、6タイプの共生細菌のうち少なくとも3タイプは土壌中に自由生活細菌として存在していることが明らかとなった。以上の結果から、外環境中の自由生活細菌がカメムシ体内に侵入し、元の共生細菌と繰り返し置き換わることで共生細菌の多型が生じたと考えられた。昆虫類の必須共生微生物の起源を示唆する重要な発見である。

  • マツヘリカメムシLeptoglossus occidentalisにおけるRickettsiaの感染状況と気温との関連

    #松本 くるみ、細川 貴弘

    第69回日本応用動物昆虫学会大会  2025.3 

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    Event date: 2025.3

    Language:Japanese  

    Venue:幕張メッセ(千葉市)   Country:Japan  

  • 南西諸島産チャバネアオカメムシ共生細菌の多様性、置換、高温感受性

    @汪亜運、細川 貴弘、@古賀 隆一、#蔡雯瑾、@森山実、@深津武馬

    第69回日本応用動物昆虫学会大会  2025.3 

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    Event date: 2025.3

    Language:Japanese  

    Venue:幕張メッセ(千葉市)   Country:Japan  

  • ツチカメムシMacroscytus japonensisにおける共生細菌の地域間の違い

    #ラモスマウロ武尊馬、#渡邊修人、細川 貴弘

    第69回日本応用動物昆虫学会大会  2025.3 

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    Event date: 2025.3

    Language:Japanese  

    Venue:幕張メッセ(千葉市)   Country:Japan  

  • ハスモンヨトウSpodoptera lituraの幼虫における昼間の潜伏行動

    #向田実央、細川 貴弘

    第69回日本応用動物昆虫学会大会  2025.3 

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    Event date: 2025.3

    Language:Japanese  

    Venue:幕張メッセ(千葉市)   Country:Japan  

  • マツヘリカメムシLeptoglossus occidentalisにおけるリケッチアの体内局在、垂直伝播様式および宿主に与える影響

    #高塚三平、#松本 くるみ、@古賀 隆一、細川 貴弘

    第69回日本応用動物昆虫学会大会  2025.3 

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    Event date: 2025.3

    Language:Japanese  

    Venue:幕張メッセ(千葉市)   Country:Japan  

  • 外来種マツヘリカメムシにおけるRickettsiaの感染状況

    #松本 くるみ、@古賀 隆一、細川 貴弘

    第68回日本応用動物昆虫学会大会  2024.3 

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    Event date: 2024.3

    Language:Japanese  

    Venue:仙台国際センター(仙台市)   Country:Japan  

  • 2つのパッチを移住する1宿主-2共生者系の動態:非同調による多様性維持

    @嶋田正和、@山道真人、@山中武彦、細川 貴弘

    第71回日本生態学会大会  2024.3 

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    Event date: 2024.3

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:オンライン(横浜市)   Country:Japan  

  • ツチカメムシと腸内細菌の共生関係維持機構

    細川貴弘、#中脇琢磨、#渡邊修人

    三学会合同大会(佐賀大会)  2023.5 

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    Event date: 2023.5

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:熊本大学(熊本市)   Country:Japan  

  • カメムシ類と腸内細菌の共生システム

    細川貴弘

    第134回日本森林学会大会  2023.3 

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    Event date: 2023.3

    Language:Japanese   Presentation type:Symposium, workshop panel (public)  

    Venue:オンライン   Country:Japan  

  • ツチカメムシMacroscytus japonensis における成長に必須な共生細菌の環境獲得

    #中脇琢磨、#渡邊修人、細川貴弘

    第67回日本応用動物昆虫学会大会  2023.3 

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    Event date: 2023.3

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:枚方   Country:Japan  

  • カメムシ類における共生細菌垂直伝播時の精巧な行動 Invited

    細川貴弘

    ERATO深津共生進化機構プロジェクト公開シンポジウム「延長された表現型の機構解明〜生物がいかにして他の生物を改変、操作するのか〜」  2023.2 

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    Event date: 2023.2

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:つくば   Country:Japan  

  • エサキモンキツノカメムシにおけるメス親の卵塊防衛

    細川貴弘、#西村航(九大・シス生)、@工藤慎一、村上貴弘

    三学会合同大会(佐賀大会)  2022.6 

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    Event date: 2022.6

    Language:Japanese   Presentation type:Oral presentation (general)  

    Country:Japan  

    ツノカメムシ科ではメス親が上に覆いかぶさる形で卵塊を保護する。この保護行動の適応的意義に関する定量的な研究はElasmucha属のみを対象としており、他属においては保護行動の断片的な報告しかない。最近の分子系統解析によって、ツノカメムシ科におけるメス親による子の保護は属ごとに独立に進化したことが明らかにされている。したがってElasmucha属以外の保護行動の適応的意義には再検討の余地がある。本研究ではSastragala属のエサキモンキツノカメムシにおける卵塊保護の適応的意義の解明および卵の捕食者の特定をおこなった。野外集団において卵塊からメス親を除去したところ、メス親を除去しない場合に比べて卵の生存率が有意に低くなった。また、メス親除去に加えて徘徊性捕食者を排除した実験では卵の生存率が有意に高くなった。メス親を除去した卵塊では卵の消失および損傷が確認され、その一因としてアリ類およびハナカメムシ類による捕食が観察された。また、今回の調査では卵寄生蜂による寄生はまったく観察されなかった。実験室内での行動観察では、メス親の体の傾けや羽ばたきがアリ類に対する防衛に有効であることが明らかとなった。

  • ミヤコキンカメムシの共生細菌の種内多型

    #鐘ヶ江正恵、#今西萌美、細川貴弘

    第66回日本応用動物昆虫学会大会  2022.3 

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    Event date: 2022.3

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:オンライン   Country:Japan  

  • チャバネアオカメムシの共生細菌はなぜ南西諸島集団だけで多様化したのか?

    #中脇琢磨、#渡邊修人、細川貴弘

    第66回日本応用動物昆虫学会大会  2022.3 

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    Event date: 2022.3

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:オンライン   Country:Japan  

  • エサキモンキツノカメムシにおけるメス親の卵塊保護行動の意義

    #西村航、@工藤慎一、細川貴弘

    第65回日本応用動物昆虫学会大会  2021.3 

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    Event date: 2021.3

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:オンライン   Country:Japan  

  • チャバネアオカメムシの野外集団では共生細菌の置換が進行しているか?:10年前と現在の比較

    細川貴弘,#今西萌美

    第65回日本応用動物昆虫学会大会  2021.3 

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    Event date: 2021.3

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:オンライン   Country:Japan  

  • エサキモンキツノカメムシのメス親は何から卵を守っているのか?

    #西村航、@工藤慎一、細川貴弘

    第39回日本動物行動学会大会  2020.11 

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    Event date: 2020.11

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:オンライン   Country:Japan  

  • キンカメムシ類における腸内共生細菌の多様化と進化

    細川貴弘、今西萌美、深津武馬

    第64回日本応用動物昆虫学会大会  2020.3 

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    Event date: 2020.3

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:名城大学   Country:Japan  

  • ツチカメムシ類(Macroscytus属)は腸内共生細菌を垂直伝播するか?

    渡邊修人、細川貴弘

    第64回日本応用動物昆虫学会大会  2020.3 

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    Event date: 2020.3

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:名城大学   Country:Japan  

  • エサキモンキツノカメムシのメス親はなぜ子を保護するのか

    西村航、工藤慎一、細川貴弘

    第64回日本応用動物昆虫学会大会  2020.3 

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    Event date: 2020.3

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:名城大学   Country:Japan  

  • ツチカメムシ類(Macroscytus属)における腸内共生細菌の多様性

    渡邊修人、細川貴弘

    第63回日本応用動物昆虫学会大会  2019.3 

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    Event date: 2019.3 - 2019.4

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:筑波大学   Country:Japan  

  • 昆虫の共生器官に複数種の細菌が同時共生しない理由-ボトルネック仮説の検証-

    今西萌美、西出雄大、深津武馬、細川貴弘

    第63回日本応用動物昆虫学会大会  2019.3 

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    Event date: 2019.3

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:筑波大学   Country:Japan  

  • カメムシの共生細菌になれる細菌となれない細菌の比較

    細川貴弘、渡邊修人、深津武馬

    日本進化学会第20回大会  2018.8 

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    Event date: 2018.8

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:東京大学   Country:Japan  

  • カメムシが複数種の細菌と同時に共生しないのはなぜか

    今西萌美、西出雄大 、深津武馬、細川貴弘

    日本進化学会第20回大会  2018.8 

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    Event date: 2018.8

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:東京大学   Country:Japan  

  • チャバネアオカメムシの共生細菌になれる環境細菌となれない環境細菌の違い

    渡邊修人、深津武馬、細川貴弘

    日本応用動物昆虫学会  2018.3 

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    Event date: 2018.5

    Language:Japanese  

    Country:Japan  

  • 複数種の細菌と同時共生しているカメムシはなぜ少ないのか

    今西萌美、西出雄大、細川貴弘

    日本応用動物昆虫学会  2018.3 

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    Event date: 2018.5

    Language:Japanese  

    Country:Japan  

  • ミナミアオカメムシではなぜ共生細菌の種内多型が生じていないのか?

    今西萌美、細川貴弘

    応用動物昆虫学会  2017.3 

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    Event date: 2017.3 - 2018.5

    Language:Japanese  

    Country:Japan  

  • ノコギリカメムシのメスの後脚に共生する菌類と産卵時の行動

    細川 貴弘, 向井裕美, 棚橋薫彦, 立川周二, 深津武馬

    日本応用動物昆虫学会  2015.3 

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    Event date: 2015.3

    Language:Japanese   Presentation type:Oral presentation (general)  

    Venue:山形   Country:Japan  

    多くの昆虫類において親は子の生存率を高めるためにさまざまな方法で子の世話をする。カメムシ類では卵の保護、栄養卵の供給、必須共生細菌を含む分泌物の供給、子への給餌などが知られている。本講演ではノコギリカメムシにおいて新たに発見した非常にユニークなメス親の行動について報告する。本種の後脚脛節には性的二型が見られ、メスではその一部が幅広く発達していた。また、この拡幅部位には性成熟にともなって菌類の菌糸束が見られるようになった。産卵時の行動を観察したところ、メス親は卵を産んだ後に後脚脛節上の菌を反対側の後脚のふ節でかきとって卵に付けた。この行動は左右交互に約2分間にわたって続き、卵を一個産下するたびに必ず繰り返された。菌を接種された卵の表面からは数日のうちにおびただしい数の菌糸が伸長して最終的には卵塊全体を被うまでに成長した。一方、メスの後脚脛節を切除することによって菌の接種を妨げると卵から菌糸が伸長することはなかった。分子系統解析の結果から、共生菌はバッカクキン科に属する子嚢菌であることが明らかになった。このメス親の行動が子の世話として機能している可能性について議論する。

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MISC

  • 土壌性カメムシの生態と腸内共生細菌

    細川貴弘

    2024.2

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    Language:Japanese   Publishing type:Article, review, commentary, editorial, etc. (scientific journal)  

  • カメムシ類の生活を栄養面で支える共生細菌

    細川 貴弘

    昆虫と自然   2015.4

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    Language:Japanese   Publishing type:Article, review, commentary, editorial, etc. (scientific journal)  

Professional Memberships

  • 日本生態学会

  • 日本応用動物昆虫学会

  • 日本動物行動学会

  • 日本進化学会

Committee Memberships

  • 日本応用動物昆虫学会   編集委員   Domestic

    2025.1 - 2025.12   

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    Committee type:Academic society

  • 日本生態学会   代議員   Domestic

    2022.1 - 2023.12   

  • 日本生態学会   代議員   Domestic

    2020.1 - 2021.12   

  • 個体群生態学会   Executive   Domestic

    2017.9 - 2019.8   

  • 日本生態学会   九州地区会事務局庶務幹事   Domestic

    2015.4 - 2025.12   

Academic Activities

  • 企画委員

    日本生態学会第70回大会  ( Japan ) 2023.3

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    Type:Competition, symposium, etc. 

  • Screening of academic papers

    Role(s): Peer review

    2023

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    Type:Peer review 

    Number of peer-reviewed articles in foreign language journals:4

  • 庶務

    日本動物行動学会第41回大会  ( Japan ) 2022.11

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    Type:Competition, symposium, etc. 

    Number of participants:200

  • 副実行委員長

    日本生態学会第69回大会  ( Japan ) 2022.3

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    Type:Competition, symposium, etc. 

  • 企画委員

    日本生態学会第69回大会  ( Japan ) 2022.3

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    Type:Competition, symposium, etc. 

  • 企画委員

    日本生態学会第68回大会  ( Japan ) 2021.3

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    Type:Competition, symposium, etc. 

  • Screening of academic papers

    Role(s): Peer review

    2021

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    Type:Peer review 

    Number of peer-reviewed articles in foreign language journals:1

  • Screening of academic papers

    Role(s): Peer review

    2020

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    Type:Peer review 

    Number of peer-reviewed articles in foreign language journals:1

  • Screening of academic papers

    Role(s): Peer review

    2019

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    Type:Peer review 

    Number of peer-reviewed articles in foreign language journals:2

  • 実行委員

    第33回個体群生態学会大会  ( Japan ) 2017.10

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    Type:Competition, symposium, etc. 

    Number of participants:109

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Research Projects

  • クロマツ採種園における害虫の実態把握と防除に関する研究

    2021.8 - 2026.3

    九州大学 

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    Authorship:Coinvestigator(s) 

  • ERATO深津共生進化機構プロジェクト

    2021.4 - 2024.3

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    Authorship:Coinvestigator(s) 

  • 昆虫類の必須共生微生物におけるゲノム進化と多様化:野外集団の追跡調査による実証

    2019.7 - 2024.3

  • 全地球規模で解き明かすカメムシ共生細菌の多様性と進化

    2019.4 - 2023.3

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    Authorship:Coinvestigator(s) 

  • 昆虫類の必須共生微生物におけるゲノム進化と多様化:野外集団の追跡調査による実証

    Grant number:19K22458  2019 - 2021

    Japan Society for the Promotion of Science  Grants-in-Aid for Scientific Research  Challenging Research(Exploratory)

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    Authorship:Principal investigator  Grant type:Scientific research funding

  • 昆虫―微生物共生可能性の探索と分子基盤の解明

    2018.3 - 2022.3

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    Authorship:Coinvestigator(s) 

  • 南西諸島で発見された新興共生細菌はどんなカメムシとも共生可能か?

    2018.3

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    Authorship:Principal investigator 

  • 全地球規模で解き明かすカメムシ共生細菌の多様性と進化

    Grant number:18KK0211  2018 - 2021

    Japan Society for the Promotion of Science  Grants-in-Aid for Scientific Research  Fostering Joint International Research (B)

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    Authorship:Coinvestigator(s)  Grant type:Scientific research funding

  • 昆虫―微生物共生可能性の探索と分子基盤の解明

    2017 - 2021

    Japan Society for the Promotion of Science・Ministry of Education, Culture, Sports, Science and Technology  Grants-in-Aid for Scientific Research  Grant-in-Aid for Scientific Research on Innovative Areas

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    Authorship:Coinvestigator(s)  Grant type:Scientific research funding

  • 南西諸島で発見された新興共生細菌はどんなカメムシとも共生可能か?

    Grant number:17H03946  2017 - 2019

    Japan Society for the Promotion of Science  Grants-in-Aid for Scientific Research  Grant-in-Aid for Scientific Research (B)

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    Authorship:Principal investigator  Grant type:Scientific research funding

  • 昆虫―大腸菌人工共生系による共生進化および分子機構の解明

    2015.4 - 2018.3

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    Authorship:Coinvestigator(s) 

  • カメムシ類の必須共生細菌はなぜ南西諸島でのみ多様化したのか?

    2015.4 - 2017.3

  • カメムシ類の必須共生細菌はなぜ南西諸島でのみ多様化したのか?

    Grant number:15K21209  2015 - 2016

    Grants-in-Aid for Scientific Research  Grant-in-Aid for Young Scientists (B)

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    Authorship:Principal investigator  Grant type:Scientific research funding

  • 昆虫―大腸菌人工共生系による共生進化および分子 機構の解明

    2013 - 2017

    Japan Society for the Promotion of Science  Grants-in-Aid for Scientific Research  Grant-in-Aid for Scientific Research (S)

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    Authorship:Coinvestigator(s)  Grant type:Scientific research funding

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Class subject

  • 進化生態学

    2025.10 - 2026.3   Second semester

  • 生物学演習I

    2025.10 - 2025.12   Fall quarter

  • 進化生態学

    2024.10 - 2025.3   Second semester

  • 生物学演習I

    2024.10 - 2024.12   Fall quarter

  • 野外実験演習

    2024.4 - 2024.9   First semester

  • 生態学実験

    2024.4 - 2024.9   First semester

  • 自然科学総合実験

    2024.4 - 2024.6   Spring quarter

  • 生物学演習Ⅰ

    2023.10 - 2023.12   Fall quarter

  • 野外実験演習

    2023.4 - 2023.9   First semester

  • 生態学実験

    2023.4 - 2023.9   First semester

  • 生物学演習Ⅰ

    2022.10 - 2022.12   Fall quarter

  • 野外実験演習

    2022.4 - 2022.9   First semester

  • 生態学実験

    2022.4 - 2022.9   First semester

  • 生物学演習Ⅰ

    2021.10 - 2021.12   Fall quarter

  • 生命の科学B

    2021.6 - 2021.8   Summer quarter

  • 野外実験演習

    2021.4 - 2021.9   First semester

  • 生態学実験

    2021.4 - 2021.9   First semester

  • 生物学演習Ⅰ

    2020.10 - 2020.12   Fall quarter

  • 生命の科学B

    2020.6 - 2020.8   Summer quarter

  • 野外実験演習

    2020.4 - 2020.9   First semester

  • 生態学実験

    2020.4 - 2020.9   First semester

  • 生命の科学B

    2019.6 - 2019.8   Summer quarter

  • 野外実験演習

    2019.4 - 2019.9   First semester

  • 生態学実験

    2019.4 - 2019.9   First semester

  • 自然科学総合実験

    2018.10 - 2019.3   Second semester

  • 生態学実験

    2018.4 - 2018.9   First semester

  • 野外実験演習

    2018.4 - 2018.9   First semester

  • 自然科学総合実験

    2017.10 - 2018.3   Second semester

  • 生態学実験

    2017.4 - 2017.9   First semester

  • 野外実験演習

    2017.4 - 2017.9   First semester

  • 生態学実験

    2016.4 - 2016.9   First semester

  • 野外実験演習

    2016.4 - 2016.9   First semester

  • 生態学実験

    2015.4 - 2015.9   First semester

  • 野外実験演習

    2015.4 - 2015.9   First semester

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Social Activities

  • 出張講義「こん虫の家族生活」

    那覇市立小学校  2024.12

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    Audience:General, Scientific, Company, Civic organization, Governmental agency

    Type:Visiting lecture

  • 出張講義「環境と生物の進化」

    筑紫女学園高等学校  2018.12

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    Audience:General, Scientific, Company, Civic organization, Governmental agency

    Type:Visiting lecture

Media Coverage

  • 著者インタビュー:カメムシの腸内共生細菌は進化の途上 Newspaper, magazine

    natureダイジェスト  2016.5

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    著者インタビュー:カメムシの腸内共生細菌は進化の途上