FY2021 Annual Report

Back row, left to right: Crystal Clitheroe, Soma Barawi, Vera Emelianenko, Kazuko Toyoda, Simon Hellemans, Nobuaki Mizumoto, Naoyuki Kuwahata. 

Front row, left to right: Tereza Berankova, Menglin Wang, Anna Prokhorova, Esra Kaymak, Cedric Aumont, Ales Bucek, Tom Bourguignon. 

The cute little boy in front: Lauro Bourguignon. 

Missing: Yukihiro Kinjo, Kensei Kikuchi, Tracy Audicio, Jigyasa Arora.



During the financial year 2021, we kept on working on the 50 termite genomes we started sequencing during FY2020. We are currently processing these data and will publish them in the coming years. We sequenced about 1000 samples of termites and cockroaches that we will use in the coming years. We also published nine peer-reviewed papers, three of which were in Nature index journals. 

1. Staff

  • Dr. Thomas Bourguignon, Assistant Professor
  • Dr. Ales Bucek, Postdoctoral Scholar
  • Dr. Yukihiro Kinjo, Postdoctoral Scholar
  • Dr. Anna Prokhorova, Postdoctoral Scholar
  • Dr. Simon Hellemans, JSPS Fellow/Postdoctoral Scholar
  • Dr. Nobuaki Mizumoto, JSPS Fellow
  • Crystal-Leigh Clitheroe, Research Unit Technician
  • Esra Kaymak, Research Unit Technician 
  • Jigyasa Arora, Ph.D. Student
  • Menglin Wang, Ph.D. Student/JRF
  • Tracy Audicio, Ph.D. Student
  • Kensei Kikuchi, Ph.D. Student
  • Kazuko Toyoda, Research Unit Administrator

2. Collaborations

2.1 Historical biogeography of termites

  • Type of collaboration: Joint research
  • Researchers:
    • Professor Yves Roisin, University of Brussels
    • Professor Nathan Lo, University of Sydney
    • Professor Rudolf A. Scheffrahn, University of Florida
    • Professor Eliana Cancello, University of Sao Paulo
    • Professor Xiaodong Yang, Xishuangbanna Tropical Botanical Gargen
    • Professor Brian Fisher, California Academy of Sciences
    • Associate Professor Jan Sobotnik, Czech University of Life Sciences
    • Associate Professor Theodore A. Evans, University of Western Australia
    • Associate Professor David Sillam-Dusses, University of Paris 13

2.2 Functional evolution of termite gut microbes

  • Type of collaboration: Joint research
  • Researchers:
    • Professor Andreas Brune, Max Planck Institute for Terrestrial Microbiology
    • Professor Nathan Lo, University of Sydney
    • Professor Gaku Tokuda, University of the Ryukyus
    • Associate Professor Jan Sobotnik, Czech University of Life Sciences

2.3 Functional evolution of termite genomes

  • Type of collaboration: Joint research
  • Researchers:
    • Associate Professor Dino McMahon, Free University of Berlin
    • Associate Professor Jan Sobotnik, Czech University of Life Sciences
    • Dr. Mark Harrison, University of Munster

3. Activities and Findings

3.1 Functional evolution of termite gut microbes

We used the gut metagenomes of 221 termite samples to investigate the functional evolution of termite gut microbes. The termite species selected are representative of termite phylogenetic and ecological diversity. This dataset allowed us to investigate the functional evolution of the gut microbiome of an entire insect order. During the fiscal year 2021, we finished writing one paper that was published at the beginning of FY2022. In this paper, we showed that (1) gut prokaryotic genes involved in the main nutritional functions and present across termites were acquired by their common ancestor; (2) the termite phylogenetic tree is largely predictive of the gut bacterial community composition and function; and (3) the acquisition of a diet of soil was accompanied by a change in the stoichiometry of genes involved in important nutritional functions rather than by the acquisition of new genes. Therefore, we shed light on the taxonomic and functional evolution of termite gut microbiota since the birth of the first termites, ~150 Million years ago (Figure 1).  

Figure 1: Relative abundance of the top 50 bacterial lineages and the major archaeal orders found in the gut metagenomes of termites. The relative abundance of prokaryotic taxa was inferred from 40 single-copy marker genes. The color scale represents the logarithm of transcripts per million (TPM). The tree represents a simplified time-calibrated phylogenetic tree reconstructed using host termite mitochondrial genome sequences. Prokaryotic taxa presenting significant phylogenetic autocorrelation with the host phylogeny at a 5% false discovery rate (FDR) are indicated with an asterisk (*p < 0.05; **p < 0.01) (reproduced from Arora et al. 2022). 

3.2 Evolution of genome size in the cockroach endosymbiont Blattabacterium

Figure 2: Evolution of genome reduction by gene loss in Blattabacterium. (A) Time-calibrated phylogenetic tree showing the evolution of genome reduction by gene loss in Blattabacterium. The tree was reconstructed with BEAST, using a set of 31 marker protein-coding genes, with third codon position excluded. Branch color represents cumulative gene loss. Node labels represent posterior distribution. Node bars indicate 95% highest posterior density. (B) Histogram representing the frequency of independent gene loss estimated from the 200 protein- coding genes lost in at least one lineage. The numbers above each bar indicate the frequency of independent gene loss. Values were derived from the reconstruction of gene loss on the maximum likelihood phylogenetic tree with branch length and were rounded to the nearest integer (see Kinjo et al. 2021).

Most cockroaches are associated with Blattabacterium, a bacterial endosymbiont providing nutrients to their hosts. Blattabacterium coevolve with their cockroach hosts and have been vertically transmitted from mother to offspring for more than 200 million years. The genomes of Blattabacterium are five to ten times smaller than that of typical free-living bacteria and keep on losing genes at a timescale of several million years. We analyzed 67 Blattabacterium genomes with the aim of determining the process of gene loss. We found that many genes were lost in parallel, with the most extreme case being one gene that was lost independently in 24 lineages (Figure 2). We identified three main mechanisms: (1) mutation rate, with gene loss rate increasing exponentially with mutation rate (Figure 3); (2) relaxed selection for genes involved in the vitamin and amino acid metabolism; and (3) epistatic interactions among genes leading to domino effect gene loss within pathways. Our results have been published during the fiscal year 2021. 

Figure 3: Exponential model investigating gene loss as a function of substitution accumulation. (A) Exponential model of gene loss and observed number of gene loss in Blattabacterium genomes. The model includes two gene-specific loss parameters: an initial gene loss rate m0 and an exponential time scale s. (B) Relationship between m0 and s for all genes in the data set. (C) Simplified phylogenetic tree of Blattabacterium. Branch colors correspond to symbol colors in (A) (see Kinjo et al. 2021).

3.3 Evolution of termite genomes

We started sequencing about 50 termite genomes during FY2019. We aim to investigate how termite genomes have evolved over the last 150 million years. We sequenced these genomes using a combination of sequencing approaches, including long reads generated with the promethION platform, short reads for polishing generated with the Illumina platform, and linked reads obtained with the Omni-C technology and sequenced on the Illumina platform. We finished the sequencing during FY2021 and started assembling the genomes. We will analyze the genomes in a comparative genomics framework during FY2022 and FY2023.

4. Publications

4.1 Journals

  1. Beránková T, Buček A, Bourguignon T, Arias JR, Akama PD, Sillam-Dussès D, et al. The ultrastructure of the intramandibular gland in soldiers of the termite Machadotermes rigidus (Blattodea: Termitidae: Apicotermitinae). Arthropod Struct Dev 2022;67:101136. https://doi.org/10.1016/j.asd.2021.101136
  2. Yashiro, T., Tea, Y.-K., Van Der Wal, C., Nozaki, T., Mizumoto, N., Hellemans, S., Matsuura, K., Lo, N. 2021. Enhanced heterozygosity from male meiotic chromosome chains is superseded by hybrid female asexuality in termites. Proceedings of the National Academy of Sciences U.S.A. 118(51): e2009533118. https://doi.org/10.1073/pnas.2009533118
  3. Mizumoto N. & Bourguignon T. The evolution of body size in termites. (2021) Proceedings of the Royal Society B, 288: 20211458, https://doi.org/10.1098/rspb.2021.1458
  4. Mizumoto N., Lee S.B., Valentini G., Chouvenc T. & Pratt S.C. (2021) Coordination of movement via complementary interactions of leaders and followers in termite mating pairs. Proceedings of the Royal Society B, 288:20210998, https://doi.org/10.1098/rspb.2021.0998
  5. Che Y., Deng W., Li W., Zhang J., Kinjo Y., Tokuda G., Bourguignon T., Lo N. & Wang Z. (2022). Vicariance and dispersal events inferred from mitochondrial genomes and nuclear genes (18S, 28S) shaped global Cryptocercus distributions. Molecular Phylogenetic and Evolution 166, 107318. https://doi.org/10.1016/j.ympev.2021.107318
  6. Sillam-Dussès D., Hradecky J., Stiblik P., Ferreira da Cunha H., Carrijo T.F., Lacey M.J., Bourguignon T. & Šobotník J. (2021) The trail-following pheromone of the termite Serritermes serrifer. Chemoecology, 31, 11-17. https://doi.org/10.1007/s00049-020-00324-2 
  7. Kinjo Y.*, Lo N.* (*equal first authors), Villa-Martin P., Tokuda G., Pigolotti S. & Bourguignon T. (2021) Enhanced mutation rate, relaxed selection, and the ‘domino effect’ are associated with gene loss in Blattabacterium, a cockroach endosymbiont. Molecular Biology and Evolution, 38, 3820-3831.https://doi.org/10.1093/molbev/msab159
  8. Beasley-Hall P.G., Rose H.A., Walker J., Kinjo Y., Bourguignon T. & Lo N. (2021) Digging deep: a revised phylogeny of Australian burrowing cockroaches (Blaberidae: Panesthiinae, Geoscapheinae) confirms extensive non-monophyly and provides insights into biogeography and evolution of burrowing. Systematic Entomology, 46, 767-783. https://doi.org/10.1111/syen.12487
  9. Romero Arias J., Boom A., Wang M., Clitheroe C., Šobotník J., Stiblik P., Bourguignon T. & Roisin Y. (2021) Molecular phylogeny and historical biogeography of Apicotermitinae (Blattodea: Termitidae). Systematic Entomology, 46, 741-756. https://doi.org/10.1111/syen.12486


4.2 Books and other one-time publications

  1. Bourguignon, T., Lo, N. Termite: phylogeny and classification. In: Starr C. (ed.) Encyclopedia of Social Insects. Springer Nature Switzerland AG. (2020)

4.3 Oral and Poster Presentations

  1. Kinjo Y. An introduction to Blattabacterium, the endosymbiont of cockroaches. 81th Annual meeting of the Entomological Society of Japan, Japan, September 2021
  2. Kinjo Y., Thomas Bourguignon. Three mechanisms driving reductive genome evolution of Blattabacterium, the endosymbiont of cockroaches. Annual meeting of Society of Genome Microbiology Japan, Japan, March 2022.
  3. Kikuchi K., Kimura A., Mitarai E., Miyazato M., & Mizumoto N. Nest is an indicator of inherent worker movements in termites. ISMMA 2021, Online, January 2022, (Poster)
  4. Lynch C., Starkey M., Pavlic P., Montgomery D., & Mizumoto N. A Study on Optimal Sampling in Multiple Social Insect Colonies with a Model-Based Approach. ABA 2021 Virtual Meeting, August  2021, (Poster)
  5. Mizumoto N., Bardunias P. M. & Pratt C. S. Parameter Tuning Facilitates the Evolution of Diverse Tunneling Patterns in Termites. DARS-SWARM 2021, Online, June 2021 (oral)
  6. Mizumoto N. Same-sex pairing is maintained by acting the other sex in termites. Ethological Society Japan, September 2021, Online
  7. Mizumoto N., Evolutionary perspectives of collective animal behavior, The Annual Meeting of the Japan Ethological Society (Tokyo) Sep. 2021 (Oral) (Invited)
  8. Mizumoto N., Comparative approach to understanding behavioral rules of termites, nest building and movement coordination, Virginia Tech University, Department of Entomology, Feb. 2022 (Invited)
  9. Mizumoto N., Evolutionary perspectives of termite collective behavior. Mississippi State University, Department of Biology, online, Feb. 2022
  10. Mizumoto N., Evolutionary perspectives of termite collective behavior. University of South Florida, Department of Integrative Biology, online, Jan. 2022
  11. Mizumoto N., Comparative analysis of behavioral rules in termites, nest building and pair movement coordination., ICMMA 2021, online, invited speaker, Jan. 2022
  12. Mizumoto N., Behavioural mechanism and its evolutionary history of termite tunnel excavation, EU-IUSSI online symposium series, Oct. 2021
  13. Mizumoto N., Same-sex pairing is maintained by acting the other sex in termites. University of St. Andrews, online, Sep. 2021
  14. Bourguignon T., Genome evolution of the cockroach endosymbiont, Blattabacterium cuenoti. Seminar in Ecology and Evolution of the Institute of Biology of the Freie Universitat Berlin, Germany. 26 April 2021.
  15. Wang M. Neoisoptera repetitively colonised Madagascar after the Middle Miocene climatic optimum. 69th Annual Meeting of Ecological Society of Japan (ESJ69). Mar. 2022. (Oral)
  16. Buček A. Convergent evolution of defensive mandibular adaptations in termites. 69th Annual Meeting of Ecological Society of Japan (ESJ69). Mar. 2022. (Oral)
  17. Prokhorova A. Long-term bioelectrochemical treatment of livestock wastewater in pilot-scale using electrotrophic bacteria. 34th Annual Meeting of the Japanese Society of Microbial Ecology (JSME). Nov. 2021. (Oral)
  18. Prokhorova A. Microenvironmental heterogeneity in gut of Nasutitermes drives differential ecological specificity and function of bacterial symbiont communities. 69th Annual Meeting of Ecological Society of Japan (ESJ69). Mar. 2022. (Oral)
  19. Mizumoto N., Bourguignon T., Bailey N., Flexible sexual role maintains same-sex pairing in termites, March 2022, Online (Poster)
  20. Bourguignon T. The functional evolution of termite gut microbiota. JSME conference (34th Annual Meeting of the Japanese Society of Microbial Ecology (JSME). Nov. 2021. (Oral, Invited))


5. Intellectual Property Rights and Other Specific Achievements​

  • Grant-in-Aid for Scientific Research (B) (Kakenhi), Japan Society for the Promotion of Science, "Elucidation of the mutation rate as driver of insect endosymbiont genome evolution", Lead PI: Bourguignon, T., Period: April 2021–March 2023
    タイトル英訳:Elucidating the dynamics and driving factors of mutation rate evolution in endosymbiotic bacteria
  • Grant-in-Aid for Early-Career Scientists, Japan Society for the Promotion of Science, "細胞内共生細菌における突然変異率の進化動態とその駆動要因の解明", Lead PI: Kinjo, Y., Period: April 2021–March 2023
    タイトル英訳:Elucidating the dynamics and driving factors of mutation rate evolution in endosymbiotic bacteria
  • The Motoo Kimura Trust Foundation for the Promotion of Evolutionary Biology, for Japan Eco-Evo English Seminar
  • 37th Inoue Research Award for Young Scientists, Grant-in-Aid for JSPS Fellows, Japan Society for the Promotion of Science, "Evolutionary process of termite construction revealed by comparative and constructive approaches", Lead PI: Mizumoto, N., Amount: 11.7M Yen, Period: April 2020–March 2023
  • Research Fellowship for Young Scientists (DC2), Japan Society for the Promotion of Science, "シロアリにおけるゲノム構造と化学受容体遺伝子族の進化", Lead PI: Tracy Audisio, Period: April 2021–March 2023
  • Grant-in-Aid for Young Scientists, Japan Society for the Promotion of Science, "シロアリにおけるゲノム構造と化学受容体遺伝子族の進化", Lead PI: Tracy Audisio, Period: April 2021–March 2023


6. Meetings and Events

6.1 Japan Eco-Evo English Seminar #1-#7


6.2 Ethological Society Japan, Round table,

アート X 動物行動学:科学の外にある表現方法の可能性, Mizumoto N., Kikuchi K.

6.3 Fundamentalz bazaar, June 2021