Elucidation of convergent evolution of genome and metagenome of primates and non-primate mammals in terms of feeding adaptation

• Project/Area Number: 19K16241
• Research Category: Grant-in-Aid for Early-Career Scientists
• Allocation Type: Multi-year Fund
• Review Section: Basic Section 45050:Physical anthropology-related
• Research Institution: Hokkaido University
• Principal Investigator: Hayakawa Takashi 北海道大学, 地球環境科学研究院, 助教 (00758493)
• Project Period (FY): 2019-04-01 – 2022-03-31
• Project Status: Completed (Fiscal Year 2021)
• Budget Amount: ¥4,160,000 (Direct Cost: ¥3,200,000、Indirect Cost: ¥960,000); Fiscal Year 2021: ¥1,300,000 (Direct Cost: ¥1,000,000、Indirect Cost: ¥300,000); Fiscal Year 2020: ¥1,300,000 (Direct Cost: ¥1,000,000、Indirect Cost: ¥300,000); Fiscal Year 2019: ¥1,560,000 (Direct Cost: ¥1,200,000、Indirect Cost: ¥360,000)
• Keywords: 採食 / 霊長類 / 有袋類 / 単孔類 / 味覚受容体 / 腸内細菌 / ゲノミクス / 収斂進化 / ゲノム / メタゲノム / 全ゲノム解析 / 樹液食 / シロアリ食 / 食性 / 化学受容体 / 味覚 / オーストラリア / 次世代シークエンサー / 比較ゲノム / 採食生態

Outline of Research at the Start

霊長類は果実食、葉食、昆虫食など、種によって食性が多様化しているのが特徴である。こうした食性の適応放散は、哺乳類全体でみられる様式の縮図ともいえる。たとえば葉を主食とするコロブス類では、ウシやヒツジ、ナマケモノ、カンガルーなどで見られる葉や草を消化する前胃の発達が見られる。本研究の目的は、こうした霊長類と非霊長類哺乳類で見られる形態・生理レベルでの採食適応の収斂のメカニズムを、ゲノム・メタゲノム適応の点から明らかにする。たとえば味覚受容体遺伝子ファミリーの分子進化（ゲノム適応）、腸内細菌叢の豊富度や構成の進化（メタゲノム適応）に着目する。

Outline of Final Research Achievements

Animals have extreme diverse diet characteristics. In addition to carnivores, omnivores, and herbivores as classical understanding, there are species-specific adaptations to a variety of feeding resources, such as folivores, frugivores, Exudivores, and nectarivores. Among the various animal taxa, primates, with around 500 species, have species with all of these diet types and are an important model of adaptive radiation in terms of feeding traits. Genomic and metagenomic adaptations were analyzed in primates and non-primate mammals with similar feeding traits under the convergent evolution, such as the exudivorous gut bacterial microbiome of slow loris (primates) vs opossum (marsupials) and taste receptor genes in the folivorous colobines (primats) vs. koala (marsupial). We found that there are evolutionary mechanisms shared between primates and non-primate mammals.

Academic Significance and Societal Importance of the Research Achievements

哺乳類の味覚や腸内細菌は、その種が消化・吸収・代謝できる食物に適している必要があり、実際そのように適応進化させてきた。各大陸に存在する森や草原や海で、異なる哺乳類が食性を収斂させている。味覚や腸内細菌は、それぞれゲノムやメタゲノムという形で分析することができ、今回、分子レベルでの収斂メカニズムを発見した。いまや4分の1の哺乳類種が絶滅の危機に瀕している中、ただ個体を保護するだけではなく、適応したゲノムやメタゲノムに基づいて、適応している森や草原といった生息地を保全する必要がある。そうした新しい形の「保全ゲノミクス」の実践を提供する上でも意義が高い研究となった。

Research Products

• [Int'l Joint Research] University of Sydney/University of Adelaide/Australian National University(オーストラリア)
• [Int'l Joint Research] University of Copenhagen(デンマーク)
• [Int'l Joint Research] 中国科学院昆明動物学研究所(中国)
• [Int'l Joint Research] Federal University of Pernambuco(ブラジル)
• [Int'l Joint Research] Bogor Agricultural University(インドネシア)
• [Int'l Joint Research]
• [Int'l Joint Research] University of Sydney/University of Adelaide/Australian Museum(オーストラリア)
• [Int'l Joint Research] University of Copenhagen(デンマーク)
• [Int'l Joint Research] BGI-Shenzhen(中国)
• [Int'l Joint Research] Federal Rural University of Pernambuco/Federal University of Pernambuco(ブラジル)
• [Int'l Joint Research] IPB University(インドネシア)
• [Journal Article] Initiation of the Primate Genome Project (2022)
  • Author(s): Wu DD, Qi XG, Yu L, Li M, Liu ZJ, Yoder AD, Roos C, Hayakawa T, Rogers J, Marques-Bonet T, Su B, Yao YG, Zhang YP, Zhang G
  • Journal Title: Zoological Research Volume: 43 Issue: 2 Pages: 147-149
  • DOI: 10.24272/j.issn.2095-8137.2022.001
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Genome assembly of the numbat (Myrmecobius fasciatus), the only termitivorous marsupial (2022)
  • Author(s): Peel Emma、Silver Luke、Brandies Parice、Hayakawa Takashi、Belov Katherine、Hogg Carolyn J.
  • Journal Title: Gigabyte Volume: 2022 Pages: 1-17
  • DOI: 10.46471/gigabyte.47
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Lowered sensitivity of bitter taste receptors to β-glucosides in bamboo lemurs: an instance of parallel and adaptive functional decline in TAS2R16? (2021)
  • Author(s): Itoigawa Akihiro、Fierro Fabrizio、Chaney Morgan E.、Lauterbur M. Elise、Hayakawa Takashi、Tosi Anthony J.、Niv Masha Y.、Imai Hiroo
  • Journal Title: Proceedings of the Royal Society B: Biological Sciences Volume: 288(1948) Issue: 1948 Pages: 20210346-20210346
  • DOI: 10.1098/rspb.2021.0346
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Lactobacillus nasalidis sp. nov., isolated from the forestomach of a captive proboscis monkey (Nasalis larvatus) (2021)
  • Author(s): Suzuki-Hashido Nami、Tsuchida Sayaka、Hayakawa Takashi、Sakamoto Mitsuo、Azumano Akinori、Seino Satoru、Matsuda Ikki、Ohkuma Moriya、Ushida Kazunari
  • Journal Title: International Journal of Systematic and Evolutionary Microbiology Volume: 71 Issue: 4 Pages: 004787-004787
  • DOI: 10.1099/ijsem.0.004787
  • Peer Reviewed
• [Journal Article] Stomach and colonic microbiome of wild Japanese macaques (2021)
  • Author(s): Lee W, Hayakawa T, Kurihara Y, Hanzawa M, Sawada A, Kaneko A, Morimitsu Y, Natsume T, Aisu S, Ito T, Honda T, Hanya G
  • Journal Title: Am J Primatol Volume: 83 Issue: 5
  • DOI: 10.1002/ajp.23242
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Phylogeographic history of Japanese macaques (2021)
  • Author(s): Ito Tsuyoshi、Hayakawa Takashi、Suzuki-Hashido Nami、Hamada Yuzuru、Kurihara Yosuke、Hanya Goro、Kaneko Akihisa、Natsume Takayoshi、Aisu Seitaro、Honda Takeaki、Yachimori Syuji、Anezaki Tomoko、Omi Toshinori、Hayama Shin‐ichi、Tanaka Mikiko、Wakamori Hikaru、Imai Hiroo、Kawamoto Yoshi
  • Journal Title: Journal of Biogeography Volume: online Issue: 6 Pages: 1-12
  • DOI: 10.1111/jbi.14087
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Early origin of sweet perception in the songbird radiation (2021)
  • Author(s): Toda Yasuka、Ko Meng-Ching、Liang Qiaoyi、Miller Eliot T.、Rico-Guevara Alejandro、Nakagita Tomoya、Sakakibara Ayano、Uemura Kana、Sackton Timothy、Hayakawa Takashi、Sin Simon Yung Wa、Ishimaru Yoshiro、Misaka Takumi、Oteiza Pablo、Crall James、Edwards Scott V.、Buttemer William、Matsumura Shuichi、Baldwin Maude W.
  • Journal Title: Science Volume: 373 Issue: 6551 Pages: 226-231
  • DOI: 10.1126/science.abf6505
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Evolution of the primate glutamate taste sensor from a nucleotide sensor (2021)
  • Author(s): Toda Yasuka、Hayakawa Takashi、Itoigawa Akihiro、Kurihara Yosuke、Nakagita Tomoya、Hayashi Masahiro、Ashino Ryuichi、Melin Amanda D.、Ishimaru Yoshiro、Kawamura Shoji、Imai Hiroo、Misaka Takumi
  • Journal Title: Current Biology Volume: 31 Issue: 20 Pages: 4641-4649
  • DOI: 10.1016/j.cub.2021.08.002
  • NAID: 120007166025
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Comparing the gut microbiome along the gastrointestinal tract of three sympatric species of wild rodents (2021)
  • Author(s): Anders Jason L.、Moustafa Mohamed Abdallah Mohamed、Mohamed Wessam Mohamed Ahmed、Hayakawa Takashi、Nakao Ryo、Koizumi Itsuro
  • Journal Title: Scientific Reports Volume: 11 Issue: 1 Pages: 19929-19929
  • DOI: 10.1038/s41598-021-99379-6
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Female chimpanzees giving first birth in their natal group in Mahale: attention to incest between brothers and sisters (2021)
  • Author(s): Matsumoto Takuya、Hanamura Shunkichi、Kooriyama Takanori、Hayakawa Takashi、Inoue Eiji
  • Journal Title: Primates Volume: 62 Issue: 2 Pages: 279-287
  • DOI: 10.1007/s10329-020-00886-3
  • NAID: 120006952819
  • Peer Reviewed
• [Journal Article] Platypus and echidna genomes reveal mammalian biology and evolution (2021)
  • Author(s): Zhou Yang、Shearwin-Whyatt Linda、Li Jing、Song Zhenzhen、Hayakawa Takashi、他
  • Journal Title: Nature Volume: NA Issue: 7856 Pages: 756-762
  • DOI: 10.1038/s41586-020-03039-0
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Evolution of the bitter taste receptor TAS2R38 in colobines. (2020)
  • Author(s): Purba LHPS, Widayati KA, Suzuki-Hashido N, Itoigawa A, Hayakawa T, Nila S, Juliandi B, Suryobroto B, Imai H.
  • Journal Title: Primates Volume: 61 Issue: 3 Pages: 485-494
  • DOI: 10.1007/s10329-020-00799-1
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Male glandular odorants attract female ring-tailed lemurs (Lemur catta): A putative pheromone in primates (2020)
  • Author(s): M. Shirasu, S. Ito, A. Itoigawa, T. Hayakawa, K. Kinoshita, I. Munechika, H. Imai, and K. Touhara
  • Journal Title: Current Biology Volume: NA Issue: 11 Pages: 2131-2138
  • DOI: 10.1016/j.cub.2020.03.037
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Fermentation Ability of Gut Microbiota of Wild Japanese Macaques in the Highland and Lowland Yakushima: In Vitro Fermentation Assay and Genetic Analyses (2020)
  • Author(s): Hanya Goro、Tackmann Janko、Sawada Akiko、Lee Wanyi、Pokharel Sanjeeta Sharma、de Castro Maciel Valdevino Gisele、Toge Akito、Kuroki Kota、Otsuka Ryoma、Mabuchi Ryoma、Liu Jie、Hatakeyama Masaomi、Yamasaki Eri、von Mering Christian、Shimizu-Inatsugi Rie、Hayakawa Takashi、Shimizu Kentaro K.、Ushida Kazunari
  • Journal Title: Microbial Ecology Volume: 80 Issue: 2 Pages: 459-474
  • DOI: 10.1007/s00248-020-01515-8
  • NAID: 120006876578
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] A natural point mutation in the bitter taste receptor TAS2R16 causes inverse agonism of arbutin in lemur gustation (2019)
  • Author(s): Itoigawa Akihiro、Hayakawa Takashi、Suzuki-Hashido Nami、Imai Hiroo
  • Journal Title: Proceedings of the Royal Society B: Biological Sciences Volume: 286 Issue: 1904 Pages: 20190884-20190884
  • DOI: 10.1098/rspb.2019.0884
  • Peer Reviewed / Open Access
• [Journal Article] Host selection of haematophagous leeches (Haemadipsa japonica): implications for iDNA studies. (2019)
  • Author(s): Hanya G, Morishima K, Koide T, Otani Y, Hongo S, Honda T, Okamura H, Higo Y, Hattori M, Kondo Y, Kurihara Y, Jin S, Otake A, Shiroisihi I, Takakuwa T, Yamamoto H, Suzuki H, Kajimura H, Hayakawa T, Suzuki-Hashido N, Nakano T.
  • Journal Title: Ecological Research Volume: 34 Issue: 6 Pages: 842-855
  • DOI: 10.1111/1440-1703.12059
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Gut microbiota composition of Japanese macaques associates with extent of human encroachment (2019)
  • Author(s): Lee Wanyi、Hayakawa Takashi、Kiyono Mieko、Yamabata Naoto、Hanya Goro
  • Journal Title: American Journal of Primatology Volume: - Issue: 12
  • DOI: 10.1002/ajp.23072
  • Peer Reviewed
• [Presentation] 飼育下の樹液食霊長類における樹液給餌と腸内細菌叢の関係について (2022)
  • Author(s): 早川卓志
  • Organizer: 第3回京都大学霊長類研究所技術部セミナー「野生から学ぶ、飼育霊長類の食事」
  • Invited
• [Presentation] 動物園由来試料を用いた霊長類のゲノム・トランスクリプトーム解析 (2022)
  • Author(s): 早川卓志
  • Organizer: 第50回ホミニゼーション研究会「人類進化と遺伝子」
• [Presentation] Comparative analysis of gut microbiome in wild- and captive-born gum-eating slow lorises (2022)
  • Author(s): Kohei Kanetsuna, Natsumi Iijima, Takashi Hayakawa.
  • Organizer: The 17th International Symposium on Primatology and Wildlife Science
  • Int'l Joint Research
• [Presentation] 毒物センサーである苦味受容体の機能と進化 (2021)
  • Author(s): 早川卓志
  • Organizer: 第48回日本毒性学会学術年会
  • Int'l Joint Research / Invited
• [Presentation] Evolution of gut microbiota in animals: Host-microbe interactions and mechanisms (2020)
  • Author(s): Takashi Hayakawa
  • Organizer: 第43回 日本分子生物学会年会
  • Int'l Joint Research
• [Presentation] Japan-Australia Wildlife Science Collaboration (2020)
  • Author(s): Takashi Hayakawa
  • Organizer: The 15th International Symposium on Primatology and Wildlife Science
  • Int'l Joint Research
• [Presentation] Genetic Origin of Koalas Captive in Japan: toward the Investigation of Innate Diet Preference (2020)
  • Author(s): Kotaro Kondo, Takashi Hayakawa
  • Organizer: The 15th International Symposium on Primatology and Wildlife Science
  • Int'l Joint Research
• [Presentation] Genetic Analysis of Captive Echidnas in Japanese Zoos using Noninvasive Spine Samples (2020)
  • Author(s): Takumi Ezawa, Takashi Hayakawa
  • Organizer: The 15th International Symposium on Primatology and Wildlife Science
  • Int'l Joint Research
• [Presentation] クモザルのるつぼ (2020)
  • Author(s): 北山遼, 白井温, 根本慧, 田和優子, 綿貫宏史朗, 早川卓志
  • Organizer: 第22回日本進化学会年大会
• [Presentation] Zoo acts as a “melting pot” of spider monkeys (2020)
  • Author(s): Haruka Kitayama, Atsushi Shirai, Kei Nemoto, Yuko Tawa, Koshiro Watanuki, Takashi Hayakawa
  • Organizer: The 14th International Symposium on Primatology and Wildlife Science
  • Int'l Joint Research
• [Presentation] 集団遺伝学的解析が明らかにした日本のクモザル類の多様性 (2020)
  • Author(s): 北山遼, 白井温, 根本慧, 田和優子, 綿貫宏史朗, 早川卓志
  • Organizer: 第36回日本霊長類学会大会
• [Presentation] ゲノムから探るグエノン類の混群形成メカニズム (2020)
  • Author(s): 北山遼, 峠明杜, 橋本千絵, 五百部裕, 今井啓雄, 古市剛史, 早川卓志
  • Organizer: 第65回プリマーテス研究会
• [Presentation] 複数種の樹液給餌により飼育下コモンマーモセットの腸内細菌叢は変動するか (2020)
  • Author(s): 金綱航平, Leonardo de Oliveira Melo, Valdir Luna da Silva, 他
  • Organizer: 第65回プリマーテス研究会
• [Presentation] 西島明日香, 栁川洋二郎, 早川卓志 (2020)
  • Author(s): クマ類における着床遅延の分子メカニズム研究
  • Organizer: 第65回プリマーテス研究会
• [Presentation] 屋久島のサル、シカ、イタチの同所的進化をゲノムから探る (2020)
  • Author(s): 早川卓志, 明石涼, 伊藤毅, 揚妻-柳原芳美, 揚妻直樹
  • Organizer: 屋久島学ソサエティ 第8回大会
• [Presentation] 御蔵島のミナミハンドウイルカ野生個体群における授乳行動の報告 (2020)
  • Author(s): 勝島日向子, 小木万布, 早川卓志
  • Organizer: 日本生態学会第68回全国大会
• [Presentation] COVID-19の拡大による観光客減少は「奈良の鹿」の腸内細菌叢を変化させたのか？ (2020)
  • Author(s): 明石涼, 石川周, 甲斐義明, 立澤史郎, 早川卓志
  • Organizer: 日本生態学会第68回全国大会
• [Presentation] Gum feeding induces short-term gut microbiome change in captive slow loris (2019)
  • Author(s): Takashi Hayakawa
  • Organizer: The 14th International Conference on Environmental Enrichment
  • Int'l Joint Research
• [Presentation] 飼育下チンパンジーにおける腸内細菌叢の多様性 (2019)
  • Author(s): 早川卓志、平田聡
  • Organizer: 第35回日本霊長類学会大会
• [Presentation] 全ゲノム解析が示すスローロリスの特殊生態の進化 (2019)
  • Author(s): 早川卓志，辰本将司，岸田拓士，鈴木彦有，樋口拓人，石川裕恵，二階堂雅人， 郷康広
  • Organizer: 日本進化学会第21回大会
• [Remarks] 北海道大学 大学院地球環境科学研究院 環境生物科学部門 生態遺伝学分野 早川研究室
  • URL: https://noah.ees.hokudai.ac.jp/hayakawa/index.html
• [Remarks] 早川研究室
  • URL: https://noah.ees.hokudai.ac.jp/hayakawa/
• [Remarks] カモノハシとハリモグラの全ゲノム解読に成功！
  • URL: https://www.hokudai.ac.jp/news/2021/01/2-48.html