FY2022

Bourguignon Unit
Associate Professor Thomas Bourguignon

(From left to right) Haruka Osaki, Terka Berankova, Simon Hellemans, Tom Bourguignon, Tracy Audisio, Cong Liu, Kensei Kikuchi, Kako Toyoda, Esra Kaymak and Nobuaki Mizumoto.

Abstract

During the financial year 2022, we kept on working on the 50 termite genomes we sequenced and assembled during FY2020 and FY2021. We carried out comparative genomics analyses on these genomes. We will publish the results in the coming years. We also sequenced >1000 termite and cockroach samples for phylogenetic purposes. We published 16 peer-reviewed papers, two of which in Nature Index journals.

1. Staff

  • Thomas Bourguignon, Associate Professor
  • Ales Bucek, Postdoctoral Scholar
  • Anna Prokhorova,  Postdoctoral Scholar
  • Simon Hellemans,  Postdoctoral Scholar
  • Nobuaki Mizumoto, JSPS Fellow
  • Esra Kaymak, Technical Staff
  • Crystal-Leigh Clitheroe, Research Unit Technician
  • Menglin Wang, JRF/VR
  • Kensei Kikuchi, Ph.D. Student
  • Tracy Audisio, Ph.D. Student
  • Cong Liu, Ph.D. Student
  • Zhuli Cheng, Ph.D. Student
  • Terka Berankova, Research Intern
  • Naoyuki Kuwahata, Research Intern
  • Soma Barawi, Research Intern
  • Himanshu Thakur, Research Intern
  • 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 Garden
    • 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 Molecular phylogeny and historical biogeography of termites

We continued working on the molecular phylogeny and historical biogeography of termites during FY2022. We specifically worked on the drywood termites, the last termite family without a comprehensive phylogenetic tree, and developed ultraconserved elements for termites.

Drywood termites are the second largest termite family, hosting one-third of termite pest species. Because a comprehensive phylogeny is still lacking for this group, we gathered molecular data (mitochondrial genomes and nuclear rRNA genes) for 172 samples, including 120 species representatives of the taxonomic diversity and geographic distribution of drywood termites, and built a robust phylogenetic tree. Our phylogenetic analyses shed light on the historical biogeography and social evolution of drywood termites. Our molecular phylogeny uncovers the timing and routes of ~40 transoceanic dispersals that led to the present-day global distribution of drywood termites (Figure 1). Our analyses show that drywood termites are particularly good at dispersing across oceans, a characteristic especially pronounced in Cryptotermes, the genus including drywood termite pest species. Our analyses support the contrarian hypothesis that the ancestor of drywood termites was socially advanced, building colonies spreading across multiple wood items and composed of individuals able to forage outside their nests (Figure 2). In contrast, species building colonies confined to a single piece of wood were found to be derived. These results show that complex society evolved early on during termite evolution, perhaps as early as in the common ancestor of all modern termites.

 

Figure 1: Time-calibrated phylogeny of Kalotermitidae. Internal node shapes summarize the congruence of all other phylogenetic analyses with the backbone tree topology. Node bars represent 95% HPD age intervals. Node pie charts represent the average probabilities of ancestral ranges. The world map indicates the biogeographic realms recognized in this study and the number of kalotermitid samples analyzed for every realm. The tree was reproduced from Buček et al. (2022).

 

Figure 2: Construction and foraging abilities of Kalotermitidae. The phylogeny from Figure 1 was collapsed at the genus level. Branches showing conflicting topology among our phylogenetic analyses are represented as polytomies. The heatmap indicates the presence of behavioral records (black) for at least one species of the genus. Note that the absence of evidence of a behavior (white) either reflects its actual absence or the absence of its observation. "Below ground level" indicates the presence of termites in wood items that are below ground level, such as tree roots. Interrogation marks indicate observations that cannot be unambiguously mapped onto the phylogeny due to the uncertain phylogenetic position of observed species. The photos show the shelter tubes of Longicaputermes sinaicus attacking timber in urban environments, the shelter tubes built by Cryptotermes brevis under laboratory conditions, and the shelter tubes built by an unidentified Glyptotermes species maintained in a laboratory and collected in Papua New Guinea. This figure was reproduced from Buček et al. (2022).

Most termite phylogenies have been reconstructed using entire mitochondrial genomes or shorter DNA sequences. While these phylogenies have improved our understanding of termite evolution, they also contain unresolved nodes that require a large number of nuclear markers to be resolved. We previously used transcriptome data to build a robust phylogenetic tree of termites with many nuclear markers (Buček et al. 2019); however, many samples stored in collections are of insufficient quality for RNA sequencing. Ultraconserved elements provide an alternative, as they can be sequenced from samples with highly degraded nucleic acids. We identified ultraconserved elements present in termite genomes and showed that they could be used to reconstruct robust termite phylogenetic trees (Figure 3). Our results will facilitate the future reconstruction of termite phylogenetic trees using many nuclear markers.

 

 

Figure 3: (A) Maximum likelihood phylogenetic tree of termites reconstructed with 5,934 UCE loci and complete mitochondrial genomes. (B) Family-level summary topology of termites supported by both UCEs (this study) and transcriptomic data (Bucek et al., 2019), with the indication of alternative topologies inferred from mitochondrial genome data alone (Bourguignon et al., 2015, 2017). Unsupported splits were summarized as polytomies (branches in red). This figure was reproduced from Hellemans et al. (2022).

 

3.2 Functional evolution of termite gut microbes

We have been investigating the functional evolution of the gut microbiome of termites using the gut metagenomes of 221 termite samples. The first paper based on this dataset was published at the beginning of FY2022 (Arora et al. 2022). This paper shed light on the taxonomic and functional evolution of termite gut microbiota since the birth of the first termites ~150 Million years ago. During FY2022, we performed additional analyses on this comprehensive dataset. We investigated the coevolution between termites and gut bacteria using cophylogenetic analyses. We built bacterial phylogenetic trees using marker genes derived from termite gut metagenomes and showed that the cophylogenetic patterns found between termites and their endemic gut bacteria can be explained by a model involving vertical transfers only (Figure 4). Our study was the first to show that horizontal transfers between termite species are not needed to explain the cophylogenetic patterns between termites and their endemic gut bacteria. Consequently, our results indicated that the symbiotic system composed of termites and their gut bacteria is the oldest case of an animal strictly cospeciating with some gut bacterial lineages. We worked on this paper during most of FY2022, and it was published during FY2023. 

 

Figure 4: Rate of transfer and phylogenetic trees of some termite-specific bacterial clades (TSCs) showing strong cophylogenetic signals with termites. (A) Rates of horizontal transfer estimated using the maximum likelihood method implemented in the GeneRax software. Tanglegrams between termites and (B) the Desulfobacterota Adiutrix TSC20, (C) the Pseudomonadota Rhodocyclaceae TSC7, and (E) the Acidobacteriota Holophagaceae TSC13. (E) Phylogenetic tree of termites inferred from mitochondrial genomes. Bacterial phylogenies were reconstructed using the marker gene COG0552. The diagrams below the phylogenetic trees indicate the results of the cophylogenetic analyses and the estimation of the horizontal transfer rate. This figure is reproduced from Arora et al. 2023, Proc. Roy. Soc. 290: 20230619).

 

4. Publications

4.1 Journals

  1. Sillam-Dussès D., Jandák V., Stiblik P., Delattre O., Chouvenc T., Balvín O., Cvačka J., Soulet D., Synek J., Brothánek M., Jiřiček O., Engel M., Bourguignon T., Šobotník J. Alarm communication predates eusociality in termites. Communication Biology, Vol. 6, pp. 83, doi: 10.1038/s42003-023-04438-5 (2023)
  2. Araujo N.S., Hellemans S., Roisin Y., Fournier D. Transcriptomic profiling of castes and of sexually and parthenogenetically produced reproductive females in the termite Cavitermes tuberosus. Entomologia Experimentalis et Applicata, Vol. 171(5), pp. 350-360, doi: 10.1111/eea.13285 (2023)
  3. Mizumoto N., Bourguignon T., Bailey W. N. Ancestral sex-role plasticity facilitates the evolution of same-sex sexual behavior. Proceedings of the National Academy of Science, Vol. 119(46), pp. e2212401119, doi: 10.1073/pnas.2212401119 (2022)
  4. Kinjo Y., Bourguignon T., Hongoh Y., Lo N., Tokuda G., Ohkuma M. Coevolution of metabolic pathways in Blattodea and their Blattabacterium endosymbionts, and comparisons with other insect-bacteria symbioses. Microbiology Spectrum, Vol. 10, pp. e02779-22, doi: 10.1128/spectrum.02779-22 (2022)
  5. Hellemans S., Šobotník J., Lepoint G., MihaljevičM., Roisin Y., Bourguignon T. Termite dispersal is influenced by their diet. Proceedings of the Royal Society B, Vol. 289, pp. 20220246. doi: 10.1098/rspb.2022.0246 (2022)
  6. Hellemans, S., Wang, M., Hasegawa, N., Šobotník, J., Scheffrahn, R.H., Bourguignon, T. Using ultraconserved elements to reconstruct the termite tree of life.  Molecular Phylogenetics and Evolution Vol. 173, pp. 107520, doi: 10.1016/j.ympev.2022.107520 (2022)
  7. Wang M., Hellemans S., Šobotník J., Arora J., Buček A., Sillam-Dussès D., Clitheroe C., Lu T., Lo N., Engel M.S., Roisin Y., Evans T.A., Bourguignon T. Historical biogeography of early diverging termite lineages (Isoptera: Teletisoptera). Systematic Entomology, Vol. 47, pp. 581-590, doi: 10.1111/syen.12548 (2022)
  8. Arora J., Kinjo Y., Šobotník J., Buček A., Clitheroe C., Stiblik P., Roisin Y., Žifčáková L., Park Y.C., Kim K.Y., Sillam-Dussès D., Herve V., Lo N., Tokuda G., Brune A., Bourguignon T. The functional evolution of termite gut microbiota. Microbiome, Vol. 10, pp. 78, doi: 10.1186/s40168-022-01258-3 (2022)
  9. Buček A., Wang M., Šobotník J., Hellemans S., Sillam-Dussès D., Mizumoto N. Stiblík, P., Clitheroe C., Lu T., González Plaza J.J., Mohagan A., Rafanomezantsoa J.J., Fisher B., Engel M., Roisin Y., Evans T.A., Scheffrahn R., Bourguignon T. Molecular phylogeny reveals the past transoceanic voyages of drywood termites (Isoptera, Kalotermitidae). Molecular Biology and Evolution, Vol. 39(5), pp. msac093, doi: 10.1093/molbev/msac093 (2022)
  10. Mizumoto N., Bourguignon T., Kanao T. Termite nest evolution fostered social parasitism by termitophilous rove beetles. Evolution, Vol. 76, pp. 1064-1072, doi: 10.1111/evo.14457 (2022)
  11. Beránková T., Buček A., Bourguignon T., Arias J.R., Akama P.D., Sillam-Dussès D., Šobotník J. The ultrastructure of the intramandibular gland in soldiers of the termite Machadotermes rigidus (Blattodea: Termitidae: Apicotermitinae). Arthropod Structure and Development, Vol. 67, 101136, doi: 10.1016/j.asd.2021.101136 (2022)
  12. Mizumoto N., Tanaka Y., Valentini G., Richardson O. T., Annagiri S., Pratt. C. S. & Shimoji H. Functional and mechanistic diversity in ant tandem runs. iScience, doi: 10.1101/2022.08.28.505613 (2022)
  13. Mizumoto N., Bourguignon T. Light alters activity but do not disturb tandem coordination of termite mating pairs. Ecological Entomology, Vol. 48, pp. 145-153, doi: 10.1111/een.13209 (2022)
  14. Lee S.B., Chouvenc T., Mizumoto N., Mullins A., Su N.Y. (2022) Age-based spatial distribution of workers is resilient to worker loss in a subterranean termite. Scientific Reports, Vol. 12, pp. 7837, doi: 10.1038/s41598-022-11512-1
  15. Mizumoto N. (2022) シロアリのランデブー探索. オペレーションズ・リサーチ, Vol. 67, pp. 167-171.
  16. Boom AF, Migliore J, Kaymak E, Meerts P, Hardy OJ (2022) Nuclear ribosomal phylogeny of Brachystegia: new markers for new insights about rain forests and Miombo woodlands evolution. Plant Ecology and Evolution, Vol. 155(2), pp. 301-314, doi: https://doi.org/10.5091/plecevo.91373 (2022)

 

4.2 Books and other one-time publications

Nothing to report

 

4.3 Oral and Poster Presentations

  1. Bourguignon T., Using phylogenetic trees to reconstruct the evolution of termites and their behavior. University Sorbonne Paris Nord. Lecture at the LEEC. 17 October 2022.
  2. Buček A., Šobotník J., Bourguignon T., Roisin Y. Evolution of symbiosis, colony organization and defense in termites. International Congress of Entomology 2022, Helsinki, Finland (Oral)
  3. Buček A., Evolutionary trajectories of mandibular snapping in termite soldier caste. 19th Congress of the International Union for the Study of Social Insects (IUSSI), July 2022, San Diego, US. (Oral)
  4. Buček A., Inferring evolution of life traits in termites without fully resolved phylogenies. OIST Mini Symposium "Phylogeny and Classification of Termites". Okinawa, Japan: Nov.-Dec. 2022. (Oral) 
  5. Hellemans S., Towards a lasting higher-level classification of termites from genomic snapshots. OIST Mini Symposium "Phylogeny and Classification of Termites". Okinawa, Japan: Nov.-Dec. 2022. (Oral)
  6. Hellemans S., Bourguignon T., Roisin Y., Patterns of population sex ratio across Isoptera. 19th Congress of the International Union for the Study of Social Insects (IUSSI), July 2022, San Diego, US. (Oral)
  7. Kikuchi K., Mizumoto N. Nest complexity reflects individual worker behavior of termites. ASAB Winter 2022, Edinburgh (UK), December 2022, (Poster)
  8. Kikuchi K., Mizumoto N. Individual termite movements reflect social complexity evolution, The 83rd Annual Meeting of the Japanese Society for Animal Psychology, Okinawa, October,  2023(Oral)
  9. Kikuchi K., Mizumoto N. Individual termite movements reflect nest complexity evolution, SHINKA2023, Okinawa, September 2023(Oral)
  10. Kikuchi K., Mizumoto N. Nest is an indicator of inherent worker movements in termites. RHINO2022, Tokyo (Japan), September 2022, (Poster)
  11. Lynch C., Starkey M., Pavlic P., Montgomery D., & Mizumoto N. Balancing within- and among-group replicates in designing experiments: Social insect research examples. 19th Congress of the International Union for the Study of Social Insects (IUSSI), July 2022, San Diego (US) (Oral)
  12. Mizumoto N., Bourguignon T., Kanao T., The evolution of termite nests promoted the invasion by termitophilous rove beetles. 19th Congress of the International Union for the Study of Social Insects (IUSSI), July 2022, San Diego (US) (Oral)
  13. Bourguignon T., Mizumoto N., Bailey N., Ancestral sex-role plasticity facilitates the evolution of same-sex sexual behavior, 19th Congress of the International Union for the Study of Social Insects (IUSSI), July 2022, San Diego (USA) (Oral)
  14. Mizumoto N., Buček A., Quantifying behavior of extinct organisms captured in amber by empirically simulating entrapment process of extant relatives. Ecological Society of Japan, March 2023, Online (Poster)
  15. Inoue T, Taniguchi J., Hung J-F, Mizumoto N., Hirai A., Takeshita F., Sato T., Kawabata Y., Evolution of sideways movements in crabs: ancestral state reconstruction of behavioral traits from extant species. Ecological Society of Japan, March 2023, Online (Poster)
  16. Inoue T, Taniguchi J., Hung J-F, Mizumoto N., Hirai A., Takeshita F., Sato T., Kawabata Y., Relationship between movement direction and morphology of Brachyuran crabs. The Annual Meeting of the Japan Ethological Society, Oct. 2022, Fukuoka Japan (Oral)
  17. Kikuchi K., Mizumoto N., 単個体の行動パターンから見るシロアリの営巣戦略の進化. The Annual Meeting of the Society of Population Ecology, Yokohama, Japan, Oct. 2022 (Poster)
  18. Kikuchi K., Mizumoto N. Nest complexity reflects individual worker behavior of termites, 70th Annual Meeting of Ecological Society of Japan, Sendai, March, 2023 (Oral)
  19. Inoue T, Taniguchi J., Hung J-F, Mizumoto N., Hirai A., Takeshita F., Sato T., Kawabata Y., カニ類における進行方向と形態の関係性の解明. The Annual Meeting of the Carcinological Society of Japan, Okayama, Japan, Sep. 2022 (Poster)
  20. Mizumoto N., Evolutionary perspectives of termite collective behavior. Auburn University, Department of Entomology and Plant Pathology, Feb. 2023 
  21. Mizumoto N., Evolution of movement coordination in termites. OIST Mini Symposium, "Phylogeny and Classification of Termites," Nov. 2022
  22. Mizumoto N., Collective Intelligence in Living/Non-Livings Populations. OIST, invited speaker, Nov. 2022
  23. Mizumoto N., Roles of Heterogeneity in Nonequilibrium Collective Dynamics. 2022 (RHINO2022), Tokyo, invited speaker, Sep. 2022
  24. Mizumoto N., シロアリの行動ルールの比較研究～集団行動の進化が知りたくて～Nagasaki University, Faculty of Fisheries, May 2022
  25. Mizumoto N., シロアリの行動ルールの比較研究～集団行動の進化が知りたくて～National Institute for Basic Biology in Japan, online, Apr. 2022 
  26. Audisio T.L., Bourguignon T. Near chromosome-level assemblies reveal that genome structure is highly conserved in termites. OIST Mini Symposium "Phylogeny and Classification of Termites". Okinawa, Japan: Nov.-Dec. 2022. (Oral)
  27. Audisio T.L., Bourguignon T. October 2022. Genome evolution in termites. OIST 3rd Joint Workshop on Biodiversity, Tohoku University, Sendai, Japan
  28. Audisio T.L., Bourguignon T. Genome evolution in termites. International Congress of Entomology 2022, Helsinki, Finland (Oral)
  29. Audisio T.L., Bourguignon T. Genome evolution in termites. 19th Congress of the International Union for the Study of Social Insects (IUSSI), July 2022, San Diego (US) (Oral)

 

5. Intellectual Property Rights and Other Specific Achievements

Nothing to report

 

6. Meetings and Events

6.1 Japan Eco-Evo English Seminar #8-#9

 

6.2 EGU Seminar: Mysterious mating behavior or a subsocial wood-feeding cockroach: female and male eat their wings one another

 1. Seminar by Dr. Haruka Osaki, Kyoto University

  • Title: Mysterious mating behavior of a subsocial wood-feeding cockroach: female and male eat their wings one another
  • Date: August 5, 2022
  • Venue: OIST Campus B503 and online

 

6.3 OIST Mini-Symposium "Physlogeny and Classification of Termites"

  • Date: November 29 - December 1, 2022
  • Venue: OIST Campus C210 and online
  • Speakers:
    • Cedric Aumont, Freie Universität Berlin
    • Dr. Thomas Chouvenc, University of Florida
    • Dr. Michael Engel, Kansas University
    • Dr. Frederic Legendre, National Museum of Natural History, France
    • Dr. Nathan Lo, University of Sydney
    • Dr. Dino Peter McMahon, Freie Universität Berlin
    • Alina Mikhailova, University of Münster
    • Dr. Yves Roisin, University of Brussels
    • Dr. Jan Šobotnik, Czech University of Life Science
    • Dr. Taisuke Kanao, Yamagata University

7. Other

Nothing to report