FY2018 Annual Report

Evolutionary Genomics Unit
Assistant Professor Thomas Bourguignon

Abstract

The Evolutionary Genomics Unit investigates the evolution and ecology of termites and cockroaches using high-throughput sequencing methods. Our main research areas presently include the evolution of symbiosis between insects and bacteria and the reconstruction of the insect tree of life. During the fiscal year 2018, we sequenced 250 mitochondrial genomes, about 20 Blattabacterium genomes, two low-coverage termite genomes, and one high-quality termite genome. We are currently processing these data and we will publish them during the coming years.

1. Staff

• Dr. Thomas Bourguignon, Assistant Professor
• Dr. Ales Bucek, Postdoctoral Scholar
• Dr. Lucia Zifcakova, Postdoctoral Scholar
• Dr. Taisuke Kanao, Postdoctoral Scholar
• Crystal-Leigh Clitheroe, Research Unit Technician
• Yukihiro Kinjo, Research Unit Technician
• Jigyasa Arora, Ph.D. Student
• Menglin Wang, Ph.D. Student
• Chihiro Arasaki, 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
  • 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
  • Professor Eliana Cancello, Curator, University of Sao Paulo

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
  • Associate Professor Jan Sobotnik, Czech University of Life Sciences

2.3 Evolution of cockroaches and their associated Blattabacterium

• Type of collaboration: Joint research
• Researchers:
  • Professor Gaku Tokuda, University of the Ryukyus
  • Professor Nathan Lo, University of Sydney

3. Activities and Findings

3.1 Historical biogeography of termites

We are using time-calibrated phylogenies to study the historical biogeography of termites. We previously studied the historical biogeography of two termite lineages: the Termitidae (Bourguignon et al. 2017) and the clade including Coptotermes, Heterotermes, and Reticulitermes (Bourguignon et al. 2016). This year, we focused on the Rhinotermitinae. We used the mitochondrial genomes of 27 species of Rhinotermitinae to build a robust time-calibrated phylogenetic tree that we used to reconstruct the ancestral distribution of the group. Our analyses support the monophyly of Rhinotermitinae and all genera of Rhinotermitinae. Our molecular clock tree indicated that Rhinotermitinae arose 50.4 Ma (41.7–60.5 Ma 95% CI). Rhinotermitinae most likely originated from the Oriental region and dispersed to other biogeographical realms. We detected four disjunctions among biogeographic realms, the earliest of which occurred 41.0 Ma (33.0–49.8 Ma 95% CI), and the latest of which occurred 20.3 Ma (15.9–25.1 Ma 95% CI). These results show that Rhinotermitinae acquired their observed distribution through a combination of transoceanic dispersals and dispersals across land bridges (Figure 1).

3.2 Mitochondrial genome phylogeny of cockroaches

Cockroaches are an ancient and widespread group of insects with a fossil record dating back 300 million years. To shed light on their evolution, we reconstructed a phylogenetic tree of all extant cockroach families based on the complete mitochondrial genomes of 117 cockroach species and 13 termites (Bourguignon et al. 2018) (Figure 2). We performed phylogenetic and divergence dating analyses and resolved, with high support, the sister group to the clade containing termites and the wood-feeding cockroach genus Cryptocercus. This sister group contains Blattidae as well as the enigmatic families Anaplectidae, Tryonicidae, and Lamproblattidae. Divergence dating analyses indicated that the last common ancestor of all extant cockroaches appeared ~220 Ma, approximately 60 Ma prior to the appearance of fossils that can be assigned to extant families and before the breakup of Pangaea began. We reconstructed the ancestral range distribution of cockroaches and found some preliminary support for vicariance through continental drift within and between a number of major lineages. We also found evidence of oceanic dispersal in seven younger lineages distributed across the Australian and Indo-Malayan regions. Our analyses provided evidence that both vicariance and dispersal have played an important role in shaping the distribution of these insects. 

3.3 Functional evolution of termite gut microbes

Termites harbor a large number of symbiotic microbes in their gut. Gut microbes provide their host with amino acids and vitamins and help digest various types of organic matter, including wood, soil, and leaf litter. Few animal groups eat wood and soil, and how they evolved to do so is still largely unknown. We are using the gut metagenomes of 221 termite samples to investigate that question. This dataset represents the first attempt to elucidate the functional evolution of the gut microbiome of an insect order. During the fiscal year 2018, we started processing the data using bioinformatics pipelines. The analyses will continue during the next fiscal year.

3.4 Evolution of cockroaches and their associated Blattabacterium

Many animals are associated with bacterial endosymbionts that participate in their metabolism. Endosymbionts have reduced genomes that evolve without gene input from outside sources. We study the evolution of cockroaches, and the evolution of the genome of Blattabacterium, the endosymbiotic bacteria of cockroaches. During the fiscal year 2018, we focused on the evolution of the genome of Blattabacterium. We showed that Blattabacterium genomes experienced parallel genome reduction in Cryptocercus and their sister group, termites (Kinjo et al. 2018). We used the full Blattabacterium genome sequence of 67 strains and determined the pace of genome evolution during the last 220 million years of Blattabacterium-cockroach coevolution. We wrote a manuscript which will be submitted during the next financial year.

4. Publications

4.1 Journals

1. Bourguignon, T.*, Qian, T.* (*equal first authors), Ho, SYW., Juna, F., Wang, Z., Arab, DA., Cameron, SL., Walker, J., Rentz, D., Evans, TA., Lo, N. Transoceanic and plate tectonics shaped global cockroach distributions: evidence from mitochondrial phylogenomics. Molecular Biology and Evolution, 35, 970-983. doi: 10.1093/molbev/msy013 (2018)
2. Kinjo, Y., Bourguignon, T., Tong, KJ., Kuwahara, H., Lim, SJ., Yoon, KB., Shigenobu, S., Park, YC., Nalepa, CA., Hongoh, Y., Ohkuma, M., Lo, N., Tokuda, G., Parallel and Gradual Genome Erosion in the Blattabacterium Endosymbionts of Mastotermes darwiniensis and Cryptocercus Wood Roaches. Genome Biology and Evolution, 10, 1622-1630. doi: 10.1093/gbe/evy110 (2018)
3. Wang, M., Bucek, A., Sobotonik, J., Sillam-Dusses, D., Evans, TA., Roisin, Y., Lo, N., Bourguignon, T., Historical biogeography of the termite clade Rhinotermitinae (Blattodea: Isoptera). Molecular Phylogenetics and Evolution, 132, 100-104. doi: 10.1016/j.ympev.2018.11.005 (2018)
4. Wu, LW., Bourguignon, T., Sobotonik, J., Wen, P., Liang, WR., Li, HF., Phylogenetic position of the enigmatic termite family Stylotermitidae (Insecta : Blattodea). Invertebrate Systematics, 32, 1111-1117. doi; 10.1071/IS17093 (2018)
5. Scheffrahn, RH., Bourguignon, T., Akama, PD., Sillam-Dusses, D., Sobotonik, J., Roisinitermes ebogoensis gen. and sp. n., an outstanding drywood termite with snapping soldiers from Cameroon (Isoptera, Kalotermitidae). ZooKeys, 787, 91-105. doi: 10.3897/zookeys.787.28195 (2018)
6. Bourguignon, T., Dahlsjo, CAL., Salim, KA., Evans, TA., Termite diversity and species composition in heath forests, mixed dipterocarp forests, and pristine and selectively logged tropical peat swamp forests in Brunei. Insects Sociaux, 65, 439-444. doi: 10.1007/s00040-018-0630-y (2018)
7. Tupec, A.*, Bucek, A.* (*equal first authors), Janousek, V., Vogel, H., Prchalova, D., Kindl, J., Pavlickova, T., Wenzelova, P., Jahn, U., Valterova, I., Pichova, I., Expansion of the fatty acyl reductase gene family shaped pheromone communication in Hymenoptera. eLife, 8, e39231. doi: 10.7554/eLife.39231 (2019)
8. Wang, M., Huang, S., Li, M., McKey, D., & Zhang, L., Staminodes influence pollen removal and deposition rates in nectar-rewarding self-incompatible Phanera yunnanensis (Caesalpinioideae). Journal of Tropical Ecology, 35, 34-42. doi:10.1017/S0266467418000433 (2019)
9. Qian, T., Bourguignon, T., Willenmse, L., De Coninck, E., Evans, T. Global spread of the German cockroach, Blattella germanica. Biological Invasions, 21, 693-707. doi: 10.1007/s10530-018-1865-2 (2019)

4.2 Books and other one-time publications

Nothing to report

4.3 Oral and Poster Presentations

1. Bourguignon, T., Lo, N., Dietrich, C., Sobotnik, J., Sidek, S., Roisin, Y., Evans, TA., Evolution of bacterial communities associated with termites. SMBE2018, Kanagawa Pref., Japan, July8–12 (2018)
2. Bucek, A., Sobotonik, J., Sillam-Dusses, D., Lo, N., Bourguignon, T., Disentangling dietary transitions in termite evolution by transcriptome- and mitochondrial genome-based phylogenies. SMBE2018, Kanagawa Pref., Japan, July8–12 (2018)
3. Kinjo, Y., Tokuda, G., Lo, N., Bourguignon, T., Large scale comparative genomics reveals the path to genome reduction in the cockroach endosymbiont, Blattabacterium. SMBE2018, Kanagawa Pref., Japan, July8–12 (2018)
4. Zifcakova, L., Bourguignon, T., Gut metagenomes reveal the evolution of lignocellulolytic abilities across termites. SMBE2018, Kanagawa Pref., Japan, July8–12 (2018)
5. Kinjo, Y., Bourguignon, T., Paths toward genome reduction in the obligate endosymbiont of cockroach, Blattabacterium. JSME 2018, Okinawa, Japan, July 13 (2018)
6. Bucek, A., Sobotonik, J., Sillam-Dusses, D., Roisin, Y., Lo, N., Bourguignon, T., Reconstructing termite evolution with transcriptome- and mitochondrial genome-based phylogenies. IUSSI 2018, Guaruja, Brazil, August 5–10 (2018)
7. Bourguignon, T., Lo, N., Sobotonik, J., Ho, SYW., Wang, M., Sillam-Dusses, D., Krizkova, B., Roisin, Y., Evans. TA., Historical Biogeography of Termites. IUSSI 2018, Guaruja, Brazil, August 5–10 (2018)
8. Kanao, T., Species Diversity and Evolution of Termitophily rove beetles. IUSSI 2018, Guaruja, Brazil, August 5–10 (2018)
9. Bourguignon, T., Shedding light on genome erosion of a 230-million-year old's cockroach friend: Blattabacterium cuenoti. The 78th Entomological Society of Japan, Aichi Pref., Japan, September 8–10 (2018)
10. Kanao, T., Maruyama, M., Evolution of termitophily and relationships with myrmecophily in the subfamily Aleocharinae (Coleoptera: Staphylinidae). The 78th Entomological Society of Japan, Aichi Pref., Japan, September 8–10 (2018)
11. Iwata, R., Kanao, T., Discovery of rove beetles of Termitohospitini from a nest of Coptotermes in Kagoshima and discussion of their biogeography. The 30th Anniversary meeting of Japanese Society of Environmental Entomology and Zoology, Kyoto, Japan, November 18 (2018)
12. Arora, J., Bourguignon, T., Metagenomics and evolution of termite gut bacteria, The 66th Annual Meeting of The Ecological Society of Japan, Hyogo, Japan, March 15–19 (2019)
13. Kanao, T., Termitophily in the rove beetle subfamily Aleocharinae, The 66th Annual Meeting of The Ecological Society of Japan, Hyogo, Japan, March 15–19 (2019)
14. Wang, M., Bourguignon, T., Worldwide Historical Biogeography of Termites (Blattodea: Isoptera), The 66th Annual Meeting of The Ecological Society of Japan, Hyogo, Japan, March 15–19 (2019)

5. Intellectual Property Rights and Other Specific Achievements

External Fundings

•  Grant-in-Aid for Yound Scientists, Japan Society for the Promotion of Science, "What is the molecular basis of parasitic manipulation in fly-termite system?", Lead PI: Bucek, A., Amount: 4.1M Yen, Period: April 2018–March 2020
• Grant-in-Aid for Yound Scientists, Japan Society for the Promotion of Science, "Shedding light on genome evolution of a 220-million-year old's cockroach friend: Blattabacterium cuenoti", Lead PI: Bourguignon, T., Amount: 3.7M Yen, Period: April 2018–MArch 2020

6. Meetings and Events

6.1 Seminars

1. Seminar by Prof. Yuichi Hongoh, School of Life Science and Technology, Tokyo Institute of Technology

• Title: Genomics of uncultivable bacteria deciphers multilayered symbiotic system in the termite gut
• Date: November 28, 2018
• Venue: OIST Campus Lab 3

2. Seminar by Prof. Yves Roisin, Evolutionary Biology and Ecology, The Free University of Brussels (ULB)

• Title: Evolution of sociality and reproductive strategies in termites
• Date: November 2, 2018
• Venue: OIST Campus Lab 3

7. Other

Nothing to report.