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Evolution of a unique defensive organ in snakes: Exploration of the developmental origin and the transitional process of prey toxin exploitation

Research Project

Project/Area Number 17H03719
Research Category

Grant-in-Aid for Scientific Research (B)

Allocation TypeSingle-year Grants
Section一般
Research Field Biodiversity/Systematics
Research InstitutionKyoto University

Principal Investigator

Mori Akira  京都大学, 理学研究科, 教授 (80271005)

Co-Investigator(Kenkyū-buntansha) 森 直樹  京都大学, 農学研究科, 教授 (30293913)
土岐田 昌和  東邦大学, 理学部, 准教授 (80422921)
Project Period (FY) 2017-04-01 – 2021-03-31
Project Status Completed (Fiscal Year 2021)
Budget Amount *help
¥17,420,000 (Direct Cost: ¥13,400,000、Indirect Cost: ¥4,020,000)
Fiscal Year 2020: ¥3,770,000 (Direct Cost: ¥2,900,000、Indirect Cost: ¥870,000)
Fiscal Year 2019: ¥3,380,000 (Direct Cost: ¥2,600,000、Indirect Cost: ¥780,000)
Fiscal Year 2018: ¥5,070,000 (Direct Cost: ¥3,900,000、Indirect Cost: ¥1,170,000)
Fiscal Year 2017: ¥5,200,000 (Direct Cost: ¥4,000,000、Indirect Cost: ¥1,200,000)
Keywords防御機構 / 毒 / 進化 / 爬虫類 / ホタル / 防御システム / 餌毒利用 / ヘビ / 形態発生
Outline of Final Research Achievements

A Japanese colubrid snake, Rhabdophis tigrinus, sequesters toxins from toads consumed as prey and stores them in the nuchal glands, which are embedded under the skin of the neck region, for the defensive use. Several congeneric species in China do not eat anurans and instead feed earthworms as main diet. We have revealed that these species also possess toxins similar to those of toads, but they sequester the toxins from fireflies, not toads. This implies that the evolution from toad-toxin utilization to firefly-toxin utilization has occurred in the ancestral species of Rhabdophis in China. In addition, we showed the morphological variation of the nuchal glands among species and clarified the diversity of the nuchal gland system in Rhabdophis.

Academic Significance and Societal Importance of the Research Achievements

毒を持つ餌を食べ、その毒を自分自身の防御に再利用する種は昆虫をはじめとする多くの動物群で知られている。ヤマカガシは餌毒を蓄積するためだけの頸腺という特殊な器官を持っているという点で、極めて珍しいヘビである。今回の研究により、毒源として利用する餌がヒキガエルからホタルへという、分類学的にも生態学的にもかけ離れた動物へ移行する進化が起こったことが示された。このような移行は他の動物群ではまったく知られていない極めて珍しい現象である。

Report

(5 results)
  • 2021 Final Research Report ( PDF )
  • 2020 Annual Research Report
  • 2019 Annual Research Report
  • 2018 Annual Research Report
  • 2017 Annual Research Report
  • Research Products

    (56 results)

All 2022 2021 2020 2019 2018 2017 Other

All Int'l Joint Research (22 results) Journal Article (10 results) (of which Int'l Joint Research: 8 results,  Peer Reviewed: 9 results,  Open Access: 8 results,  Acknowledgement Compliant: 1 results) Presentation (23 results) (of which Int'l Joint Research: 7 results,  Invited: 1 results) Book (1 results)

  • [Int'l Joint Research] 成都生物研究所/楽山師範大学(中国)

    • Related Report
      2020 Annual Research Report
  • [Int'l Joint Research] ボゴール動物学博物館(インドネシア)

    • Related Report
      2020 Annual Research Report
  • [Int'l Joint Research] ユタ州立大学(米国)

    • Related Report
      2020 Annual Research Report
  • [Int'l Joint Research] スリ・ジャヤワルデネプラ大学(スリランカ)

    • Related Report
      2020 Annual Research Report
  • [Int'l Joint Research] サラワク大学(マレーシア)

    • Related Report
      2020 Annual Research Report
  • [Int'l Joint Research] 成都生物研究所/楽山師範大学(中国)

    • Related Report
      2019 Annual Research Report
  • [Int'l Joint Research] ボゴール動物学博物館(インドネシア)

    • Related Report
      2019 Annual Research Report
  • [Int'l Joint Research] ユタ州立大学(米国)

    • Related Report
      2019 Annual Research Report
  • [Int'l Joint Research] スリ・ジャヤワルデネプラ大学(スリランカ)

    • Related Report
      2019 Annual Research Report
  • [Int'l Joint Research] サラワク大学(マレーシア)

    • Related Report
      2019 Annual Research Report
  • [Int'l Joint Research]

    • Related Report
      2019 Annual Research Report
  • [Int'l Joint Research] 成都生物研究所/楽山師範大学(中国)

    • Related Report
      2018 Annual Research Report
  • [Int'l Joint Research] ボゴール動物学博物館(インドネシア)

    • Related Report
      2018 Annual Research Report
  • [Int'l Joint Research] ユタ州立大学(米国)

    • Related Report
      2018 Annual Research Report
  • [Int'l Joint Research] スリ・ジャヤワルデネプラ大学(スリランカ)

    • Related Report
      2018 Annual Research Report
  • [Int'l Joint Research] サラワク大学(マレーシア)

    • Related Report
      2018 Annual Research Report
  • [Int'l Joint Research] ユタ州立大学(米国)

    • Related Report
      2017 Annual Research Report
  • [Int'l Joint Research] 中国科学院成都生物研究所/楽山師範大学(中国)

    • Related Report
      2017 Annual Research Report
  • [Int'l Joint Research] 国立ピントン科技大学(台湾)

    • Related Report
      2017 Annual Research Report
  • [Int'l Joint Research] インドネシア科学院ボゴール動物学博物館(インドネシア)

    • Related Report
      2017 Annual Research Report
  • [Int'l Joint Research] ベトナム国立自然博物館(ベトナム)

    • Related Report
      2017 Annual Research Report
  • [Int'l Joint Research]

    • Related Report
      2017 Annual Research Report
  • [Journal Article] Do predators prefer toxic animals? A case of chemical discrimination by an Asian snake that sequesters firefly toxins2022

    • Author(s)
      Fukuda Masaya、Ujiie Rinako、Inoue Takato、Chen Qin、Cao Chengquan、Ding Li、Mori Naoki、Mori Akira
    • Journal Title

      Current Zoology

      Volume: 未定 Issue: 6 Pages: 1-8

    • DOI

      10.1093/cz/zoab102

    • Related Report
      2020 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Cryptic diversity and phylogeography of the Rhabdophis nuchalis group (Squamata: Colubridae)2022

    • Author(s)
      Zhu Guangxiang、Yang Shijun、Savitzky Alan H.、Cheng Yuqi、Mori Akira、Ding Li、Rao Dingqi、Wang Qin
    • Journal Title

      Molecular Phylogenetics and Evolution

      Volume: 166 Pages: 107325-107325

    • DOI

      10.1016/j.ympev.2021.107325

    • Related Report
      2020 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Does an Asian Natricine Snake, <i>Rhabdophis tigrinus</i>, Have Chemical Preference for a Skin Toxin of Toads?2021

    • Author(s)
      Fukuda, M. and Mori, A.
    • Journal Title

      Current Herpetology

      Volume: 40 Issue: 1 Pages: 1-9

    • DOI

      10.5358/hsj.40.1

    • NAID

      130007992258

    • ISSN
      1345-5834, 1881-1019
    • Related Report
      2020 Annual Research Report
    • Peer Reviewed
  • [Journal Article] New Insights Into Dietary Toxin Metabolism: Diversity in the Ability of the Natricine Snake Rhabdophis tigrinus to Convert Toad-Derived Bufadienolides2021

    • Author(s)
      Inoue Takato、Nakata Ryu、Savitzky Alan H.、Yoshinaga Naoko、Mori Akira、Mori Naoki
    • Journal Title

      Journal of Chemical Ecology

      Volume: 47 Issue: 10-11 Pages: 915-925

    • DOI

      10.1007/s10886-021-01287-6

    • Related Report
      2020 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Dramatic dietary shift maintains sequestered toxins in chemically defended snakes2020

    • Author(s)
      Tatsuya Yoshida, Rinako Ujiie, Alan H. Savitzky, Teppei Jono, Takato Inoue, Naoko Yoshinaga, Shunsuke Aburaya, Wataru Aoki, Hirohiko Takeuchi, Li Ding, Qin Chen, Chengquan Cao, Tein-Shun Tsai, Anslem de Silva, Dharshani Mahaulpatha, Tao Thien Nguyen, Yezhong Tang, Naoki Mori, and Akira Mori
    • Journal Title

      Proceedings of the National Academy of Sciences

      Volume: 117 Issue: 11 Pages: 5964-5969

    • DOI

      10.1073/pnas.1919065117

    • NAID

      120006800720

    • Related Report
      2019 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] 生物が作り出す毒:どくどくしくない毒のはなし2020

    • Author(s)
      山下まり・此木敬一・稲垣英利・森 直樹・森 哲
    • Journal Title

      化学と生物

      Volume: 58 Pages: 43-59

    • NAID

      130007979405

    • Related Report
      2019 Annual Research Report
  • [Journal Article] Evolution of nuchal glands, unusual defensive organs of Asian natricine snakes (Serpentes: Colubridae), inferred from a molecular phylogeny2019

    • Author(s)
      Takeuchi, H., A. H. Savitzky, L. Ding, A. de Silva, I. Das, T. T. Nguyen, T.-S. Tsai, T. Jono, G.-X. Zhu, D. Mahaulpatha, Y. Tang, and A. Mori
    • Journal Title

      Ecology and Evolution

      Volume: 8 Issue: 20 Pages: 10219-10232

    • DOI

      10.1002/ece3.4497

    • Related Report
      2018 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Snakes exhibit tissue-specific variation in cardiotonic steroid sensitivity of Na+/K+-ATPase2018

    • Author(s)
      Mohammadi, S., G. Petschenka, S. S. French, A. Mori, and A. H. Savitzky
    • Journal Title

      Comparative Biochemistry and Physiology, Part B

      Volume: 217 Pages: 21-26

    • DOI

      10.1016/j.cbpb.2017.11.014

    • Related Report
      2017 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Corticosteroid responses of snakes to toxins from toads (bufadienolides) and plants (cardenolides) reflect differences in dietary specializations2017

    • Author(s)
      Mohammadi, S., S. S. French, L. A. Neuman-Lee, S. L. Durham, Y. Kojima, A. Mori, E. D. Brodie Jr., and A. H. Savitzky
    • Journal Title

      General and Comparative Endocrinology

      Volume: 247 Pages: 16-25

    • DOI

      10.1016/j.ygcen.2017.03.015

    • Related Report
      2017 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research / Acknowledgement Compliant
  • [Journal Article] Do tiger keelback snakes (Rhabdophis tigrinus) recognize how toxic they are?2017

    • Author(s)
      Mori, A. and G. M. Burghardt
    • Journal Title

      Journal of Comparative Psychology

      Volume: 131 Issue: 3 Pages: 257-265

    • DOI

      10.1037/com0000075

    • Related Report
      2017 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Presentation] 毒源が変われば形態も変わる?ー食性の異なるヤマカガシ属における頭部形態の変化2022

    • Author(s)
      福田将矢、Jing-Song Shi、Alan H. Savitzky、Qin Chen、森哲
    • Organizer
      第69回日本生態学会大会
    • Related Report
      2020 Annual Research Report
  • [Presentation] ヤマカガシ属ヘビが保有する強心性ステロイドの種間差異2022

    • Author(s)
      井上 綾、井上貴斗、吉永直子、森哲、森直樹
    • Organizer
      日本農芸化学会2022年度大会
    • Related Report
      2020 Annual Research Report
  • [Presentation] ヤマカガシにおけるエサ由来毒素変換能力の多様性2022

    • Author(s)
      井上貴斗、吉永直子、森 哲、森直樹
    • Organizer
      日本農芸化学会2022年度大会
    • Related Report
      2020 Annual Research Report
  • [Presentation] ヤマカガシにおける「毒源生物」の化学認知に関する研究2021

    • Author(s)
      福田将矢、井上貴斗、森直樹、森哲
    • Organizer
      第40回日本動物行動学会大会
    • Related Report
      2020 Annual Research Report
  • [Presentation] ヤマカガシにおける「毒源生物」の化学認知に関する研究2021

    • Author(s)
      福田将矢、井上貴斗、森直樹、森哲
    • Organizer
      日本爬虫両棲類学会第60回大会
    • Related Report
      2020 Annual Research Report
  • [Presentation] How predators recognize toxic animals as a toxin source: A case of chemical discrimination by an Asian snake that sequesters firefly toxins2021

    • Author(s)
      Masaya Fukuda, Qin Chen, Akira Mori
    • Organizer
      International Conference on Herpetological Biodiversity and Conservation in Eurasian Countries
    • Related Report
      2020 Annual Research Report
    • Int'l Joint Research
  • [Presentation] ヤマカガシにおけるヒキガエル由来毒素変換能力の多様性2021

    • Author(s)
      井上貴斗, 中田隆, Alan H. Savitzky, 吉永直子, 森哲, 森直樹
    • Organizer
      日本農芸化学会 西日本・中四国・関西支部合同大会
    • Related Report
      2020 Annual Research Report
  • [Presentation] Toads or fireflies? Which do Asian natricine snakes prefer as a source of steroidal toxins?2020

    • Author(s)
      Fukuda M., Mori A., and Chen Q.
    • Organizer
      The 9th World Congress of Herpetology
    • Related Report
      2019 Annual Research Report
    • Int'l Joint Research
  • [Presentation] ヤマカガシ(Rhabdophis tigrinus) が有する頸腺毒成分の地域的特徴2020

    • Author(s)
      井上貴斗、中田隆、吉永直子、Alan H. Savitzky、森哲、森直樹
    • Organizer
      2020年度日本農芸化学会
    • Related Report
      2019 Annual Research Report
  • [Presentation] 中国産ヤマカガシ類の頸腺毒の由来および頭部の形態変化に関する考察2020

    • Author(s)
      福田将矢・井上貴斗・Alan Savitsky・Piao Yige・城野哲平・Chen Qin・森直樹・森哲
    • Organizer
      第67回日本生態学会大会
    • Related Report
      2019 Annual Research Report
  • [Presentation] Does an Asian natricine snake recognize fireflies that have cardiac steroidal toxins?2019

    • Author(s)
      Fukuda M., Mori A., and Chen Q.
    • Organizer
      The 36th International Ethological Conference
    • Related Report
      2019 Annual Research Report
    • Int'l Joint Research
  • [Presentation] Unexpected origins of defensive compounds in animals2019

    • Author(s)
      Naoki MORI and Akira MORI
    • Organizer
      The 10th Conference of Asia-Pacific Association of Chemical Ecologists
    • Related Report
      2019 Annual Research Report
    • Int'l Joint Research / Invited
  • [Presentation] ヒキガエルかホタルか?中国産ヤマカガシ類の頸腺毒の由来に関する考察2019

    • Author(s)
      福田将矢・井上貴斗・Piao Yige・Chen Qin・森直樹・森哲
    • Organizer
      日本爬虫類両棲類学会第58回大会
    • Related Report
      2019 Annual Research Report
  • [Presentation] 中国産ヤマカガシ類は毒を持つホタルを選択的に捕食するのか?2019

    • Author(s)
      福田将矢・森哲・Chen Qin
    • Organizer
      日本動物行動学会第37回大会
    • Related Report
      2018 Annual Research Report
  • [Presentation] A study of Rhabdophis in Indonesia: an effort to identify presence of the Nuchal Gland2019

    • Author(s)
      Syahfitri Anita, Amir Hamidy, Misbahul Munir, Akira Mori
    • Organizer
      日本爬虫両棲類学会第57回大会
    • Related Report
      2018 Annual Research Report
  • [Presentation] ヤマカガシ属ヘビ Rhabdophis pentasupralabialis が頸腺に蓄積するステロイド毒の由来2019

    • Author(s)
      氏家里奈子・吉田達哉・竹内寛彦・城野哲平・Qin Chen・Li Ding・Yezhong Tang・Tsai Tein-Shun・Cao Chengquan・Alan Savitzky・森哲・森直樹
    • Organizer
      日本爬虫両棲類学会第57回大会
    • Related Report
      2018 Annual Research Report
  • [Presentation] 中国産ヤマカガシ類は毒を持つホタルを選択的に捕食するのか?2019

    • Author(s)
      福田将矢・森哲・Chen Qin
    • Organizer
      日本爬虫両棲類学会第57回大会
    • Related Report
      2018 Annual Research Report
  • [Presentation] ヤマカガシ属ヘビ Rhabdophis pentasupralabialis が蓄積する毒性ステロイド bufadienolide の由来2019

    • Author(s)
      氏家 里奈子、竹内 寛彦、城野 哲平、チェン チン、ディン リー、タン イェチョン、ツァイ テインシュン、ツァオ チェンチャン、アラン サビツキー、油屋 駿介、青木 航、吉永 直子、森 哲、森 直樹
    • Organizer
      日本農芸化学会2019年度大会
    • Related Report
      2018 Annual Research Report
  • [Presentation] ヒキガエルが持つステロイド毒 bufadienolide 類の化学分析2019

    • Author(s)
      井上 貴斗、氏家 里奈子、吉永 直子、森 哲、森 直樹
    • Organizer
      日本農芸化学会2019年度大会
    • Related Report
      2018 Annual Research Report
  • [Presentation] The chemical analysis of bufadienolides in defensive glands of the Asian Rhabdophis snakes2017

    • Author(s)
      Tatsuya Yoshida, Teppei Jono , Hirohiko Takeuchi, Rinako Ujiie, Naoko Yoshinaga, Li Ding, Yezhong Tang, Akira Mori, Naoki Mori
    • Organizer
      The Joint Meeting of the 33rd Annual Meeting of the International Society of Chemical Ecology and the 9th Meeting of Asia-Pacific Association of Chemical Ecology
    • Related Report
      2017 Annual Research Report
    • Int'l Joint Research
  • [Presentation] Mechanisms of resistance to bufadienolide toxins in toad-eating snakes2017

    • Author(s)
      Alan H. Savitzky, Shabnam Mohammadi, Susanne Dobler, Zachariah Gompert, Georg Petschenka, Akira Mori
    • Organizer
      The Joint Meeting of the 33rd Annual Meeting of the International Society of Chemical Ecology and the 9th Meeting of Asia-Pacific Association of Chemical Ecology
    • Related Report
      2017 Annual Research Report
    • Int'l Joint Research
  • [Presentation] Chemical analysis of bufadienolides in Japanese Lampyrine fireflies2017

    • Author(s)
      Rinako Ujiie, Tatsuya Yoshida, Hirohiko Takeuchi, Koshiro Eto, Teppei Jono, Naoko Yoshinaga, Akira Mori, Naoki Mori
    • Organizer
      The Joint Meeting of the 33rd Annual Meeting of the International Society of Chemical Ecology and the 9th Meeting of Asia-Pacific Association of Chemical Ecology
    • Related Report
      2017 Annual Research Report
    • Int'l Joint Research
  • [Presentation] ヤマカガシはヒキガエル毒に嗜好性を示すのか?―ヒキガエル食からホタル食への変遷の要因を探る―2017

    • Author(s)
      福田将矢・森哲
    • Organizer
      日本爬虫両棲類学会第56回大会
    • Related Report
      2017 Annual Research Report
  • [Book] APA Handbook of Comparative Psychology Volume 1. (J. Call, ed.), Chapter 40, Antipredator Behavior2017

    • Author(s)
      Mori, A. and R. Ito
    • Publisher
      American Psychological Association
    • ISBN
      1433823500
    • Related Report
      2017 Annual Research Report

URL: 

Published: 2017-04-28   Modified: 2023-01-30  

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