Genetic mechanism of parallel evolution of mimicry supergene in swallowtail butterflies

• Project/Area Number: 20H00474
• Research Category: Grant-in-Aid for Scientific Research (A)
• Allocation Type: Single-year Grants
• Section: 一般
• Review Section: Medium-sized Section 45:Biology at organismal to population levels and anthropology, and related fields
• Research Institution: The University of Tokyo
• Principal Investigator: Fujiwara Haruhiko 東京大学, 大学院新領域創成科学研究科, 教授 (40183933)
• Project Period (FY): 2020-04-01 – 2023-03-31
• Project Status: Completed (Fiscal Year 2022)
• Budget Amount: ¥40,560,000 (Direct Cost: ¥31,200,000、Indirect Cost: ¥9,360,000); Fiscal Year 2022: ¥13,390,000 (Direct Cost: ¥10,300,000、Indirect Cost: ¥3,090,000); Fiscal Year 2021: ¥13,390,000 (Direct Cost: ¥10,300,000、Indirect Cost: ¥3,090,000); Fiscal Year 2020: ¥13,780,000 (Direct Cost: ¥10,600,000、Indirect Cost: ¥3,180,000)
• Keywords: スーパージーン / 擬態 / アゲハチョウ / 平行進化 / 遺伝子機能 / 染色体逆位 / 相同組換え / アゲハ蝶

Outline of Research at the Start

体表の紋様や体色によって捕食者を攪乱する擬態は広範な動物にみられる。擬態などの複雑な適応形質には、染色体上の隣接遺伝子群「超遺伝子（スーパージーン）」が制御しているものがある。シロオビアゲハとナガサキアゲハという近縁な2種の蝶はベイツ型擬態をする。その原因領域はいずれもスーパージーン構造をもつが、その構造や主要遺伝子の比較から両者は独立に平行進化したと考えられた。本研究では、アゲハチョウ属のベイツ型擬態の平行進化とスーパージーンの遺伝的背景を明らかにする。

Outline of Final Research Achievements

Some complex adaptive traits, such as mimicry, are controlled by groups of contiguous genes on a chromosome called ``supergene''. Chromosomal inversions suppress recombination in many supergenes, such as the region responsible for Batesian mimicry in Papilio polytes, but are absent in a mimicry supergene in the closely related Papilio machaon. In this study, we clarified for the first time that multiple genes that constitute the mimicry supergenes of these two species are involved in mimicry pattern formation. In addition, we clarified the genetic background and evolutionary process of parallel evolution of Batesian mimicry by comparing the structures of mimicry supergenes of related species of swallowtails.

Academic Significance and Societal Importance of the Research Achievements

スーパージーンは90年以上前に提唱された遺伝学的概念だが、その実体についてはほとんど実証されていなかった。近年、ゲノム解析の劇的な進展により、数多くの複雑な適応形質がスーパージーンで制御されていることが明らかになったが、スーパージーン内の遺伝子の機能や逆位の役割が明瞭になったものはない。本研究は、スーパージーン内外の複数の遺伝子が適応形質を生み出していること、さらに逆位の外側の遺伝子も形質発現に関与していることを、スーパージーンでは初めて実証した。また、シロオビアゲハとナガサキアゲハの擬態スーパージーンがどのように進化したかをゲノム構造の比較から明瞭にした。

Research Products

• [Journal Article] Functional unit of supergene in female-limited Batesian mimicry of Papilio polytes (2023)
  • Author(s): Komata Shinya、Yoda Shinichi、KonDo Yusuke、Shinozaki Souta、Tamai Kouki、Fujiwara Haruhiko
  • Journal Title: Genetics Volume: 223 Issue: 2
  • DOI: 10.1093/genetics/iyac177
  • Peer Reviewed
• [Journal Article] Genomic architecture and functional unit of mimicry supergene in female limited Batesian mimic Papilio butterflies. (2022)
  • Author(s): Komata S, Kajitani R, Itoh T, Fujiwara H.
  • Journal Title: Philosophical Transactions of the Royal Society B Volume: - Issue: 1856 Pages: 20210198-20210198
  • DOI: 10.1098/rstb.2021.0198
  • Peer Reviewed / Open Access
• [Journal Article] doublesex Controls Both Hindwing and Abdominal Mimicry Traits in the Female-Limited Batesian Mimicry of Papilio memnon (2022)
  • Author(s): Shinya Komata、Chung-Ping Lin、Haruhiko Fujiwara
  • Journal Title: Frontiers in Insect Science Volume: 2
  • DOI: 10.3389/finsc.2022.929518
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Dimorphic Female-Limited Batesian Mimicry in Two Papilio Butterflies (2022)
  • Author(s): Fujiwara Haruhiko、Komata Shinya
  • Journal Title: Spectrum of Sex: The Molecular Bases that Induce Various Sexual Phenotypes Volume: book Pages: 37-52
  • DOI: 10.1007/978-981-19-5359-0_3
  • ISBN: 9789811953583, 9789811953590
  • Peer Reviewed
• [Journal Article] Electroporation can be used to explore the gene function in the silkworm, Bombyx mori. , 64 (7), (2021)
  • Author(s): ZHOU Wen-Lin, Haruhiko FUJIWARA, Nozomi UEMURA, YE Ai-Hong, WU Xue-Hui, CHEN Xue-Dong, ZHANG Ting-Ting, CAO Jin-RuSyu
  • Journal Title: Acta Entomologica Sinica Volume: 64 Pages: 809-816
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Genetic switch in UV response of mimicry-related pale-yellow colors in Batesian mimic butterfly, Papilio polytes (2021)
  • Author(s): Yoda, S. Sakakura, K., Kitamura, T., KonDo, Y., Sato, K., Ohnuki, R., Someya, T., Komata, S., Kojima, T., Yoshioka, S. and Fujiwara, H.
  • Journal Title: Science Advances Volume: 7 Issue: 2
  • DOI: 10.1126/sciadv.abd6475
  • Peer Reviewed / Open Access
• [Journal Article] A corset function of exoskeletal ECM promotes body elongation in Drosophila. (2021)
  • Author(s): Tajiri, R., Fujiwara, H., Kojima, T.
  • Journal Title: Communications Biology Volume: 4 Issue: 1 Pages: 1-13
  • DOI: 10.1038/s42003-020-01630-9
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] 紫外線を使って毒チョウに擬態するアゲハ (2021)
  • Author(s): 藤原晴彦
  • Journal Title: 化学 Volume: 76 Pages: 72-72
• [Journal Article] スーパージーンによる不思議な進化 (2021)
  • Author(s): 藤原晴彦
  • Journal Title: ニューサポート高校理科 Volume: 36 Pages: 8-9
• [Journal Article] Molecular mechanisms underlying pupal protective color switch in Papilio polytes butterflies. (2020)
  • Author(s): Yoda, S., Otaguro, E. Nobuta, M. and Fujiwara, H.
  • Journal Title: Front.Ecol.Evol. Volume: 8 Pages: 51-51
  • DOI: 10.3389/fevo.2020.00051
  • Peer Reviewed / Open Access
• [Journal Article] Notch and delta control the switch and formation of camouflage patterns in caterpillars (2020)
  • Author(s): Jin, H., Yoda, S. Liu, L., Kojima, T. and Fujiwara, H.
  • Journal Title: iScience Volume: 23 Issue: 7 Pages: 101315-101315
  • DOI: 10.1016/j.isci.2020.101315
  • Peer Reviewed / Open Access
• [Journal Article] Essential factors involved in the precise targeting and insertion of telomere-specific non-LTR retrotransposon, SART1Bm. (2020)
  • Author(s): Nichuguti, N. and Fujiwara, H.
  • Journal Title: Scientific Reports Volume: 10 Issue: 1 Pages: 8963-8963
  • DOI: 10.1038/s41598-020-65925-x
  • Peer Reviewed / Open Access
• [Journal Article] Batesian mimicry has evolved with deleterious effects of the pleiotropic gene doublesex (2020)
  • Author(s): Komata S, Kitamura T, Fujiwara H.
  • Journal Title: Scientific Reports Volume: 10 Issue: 1 Pages: 21333-21333
  • DOI: 10.1038/s41598-020-78055-1
  • Peer Reviewed / Open Access
• [Presentation] アゲハチョウ属のメスに限られたベイツ型擬態を制御するスーパージーンの機能と進化 (2022)
  • Author(s): 古俣慎也、依田真一、梶谷嶺、篠崎颯太、藤原晴彦
  • Organizer: 第24回日本進化学会
• [Presentation] Functional unit and evolutionary process of mimicry supergene in Papilio butterflies. (2022)
  • Author(s): Fujiwara, Haruhiko & Komata Shinya
  • Organizer: The 11th International Workshop on Molecular Biology and Genetics of the Lepidoptera
  • Int'l Joint Research
• [Presentation] Functional unit and evolutionary process of mimicry supergene in Papilio butterflies. (2022)
  • Author(s): Fujiwara, Haruhiko & Komata, Shinya
  • Organizer: The 11th International Workshop on Molecular Biology and Genetics of the Lepidoptera
  • Int'l Joint Research
• [Presentation] アゲハチョウの前翅/後翅のアイデンティティを決定する段階的な発生運命機構 (2021)
  • Author(s): 依田真一、篠崎颯太、吉岡伸也、藤原晴彦
  • Organizer: 第23回日本進化学会
• [Presentation] ECMの変形による形づくり：ショウジョウバエ外骨格を例として (2021)
  • Author(s): 田尻怜子、藤原晴彦、小嶋徹也
  • Organizer: 第42回日本分子生物学会年会
• [Presentation] Co-expression of JH binding protein and Bilin binding protein contributes to the accumulation of green pigments in Papilio memnon. (2021)
  • Author(s): Liang Liu, Shinya Komata, Haruhiko Fujiwara
  • Organizer: 第42回日本分子生物学会年会
• [Presentation] シロオビアゲハの擬態を制御するスーパージーン内部遺伝子の発現動態と機能解析 (2021)
  • Author(s): 篠﨑颯太、依田真一、古俣慎也、田中智大、藤原晴彦
  • Organizer: 第42回日本分子生物学会年会
• [Presentation] ゼブラフィッシュrDNAに転移する2種類の標的特的レトロトランスポゾンの転移解析 (2020)
  • Author(s): 鍜治桃子、朴享道、比嘉真鈴、藤原晴彦
  • Organizer: 第41回日本分子生物学会年会
• [Presentation] Insect body shape sculpted by cuticle deromation (2020)
  • Author(s): Reiko Tajiri, Haruhiko Fujiwara, Tetsuya Kojima
  • Organizer: 第41回日本分子生物学会年会
• [Book] マーダー生物学 (2021)
  • Author(s): S. Mader、藤原 晴彦
  • Total Pages: 560
  • Publisher: 東京化学同人
  • ISBN: 9784807909698
• [Book] ヒトゲノム事典 (2021)
  • Author(s): 藤原晴彦（分担執筆）
  • Total Pages: 448
  • Publisher: 一色出版
  • ISBN: 9784910389127
• [Book] カイコの科学 (2020)
  • Author(s): 藤原晴彦（分担執筆）
  • Total Pages: 224
  • Publisher: 朝倉書店
  • ISBN: 9784254420432