Genomic data provide insights into the classification of extant termites

Simon Hellemans, Mauricio M. Rocha, Menglin Wang, Johanna Romero Arias, Duur K. Aanen, Anne Geneviève Bagnères, Aleš Buček, Tiago F. Carrijo, Thomas Chouvenc, Carolina Cuezzo, Joice P. Constantini, Reginaldo Constantino, Franck Dedeine, Jean Deligne, Paul Eggleton, Theodore A. Evans, Robert Hanus, Mark C. Harrison, Myriam Harry, Guy JosensCorentin Jouault, Chicknayakanahalli M. Kalleshwaraswamy, Esra Kaymak, Judith Korb, Chow Yang Lee, Frédéric Legendre, Hou Feng Li, Nathan Lo, Tomer Lu, Kenji Matsuura, Kiyoto Maekawa, Dino P. McMahon, Nobuaki Mizumoto, Danilo E. Oliveira, Michael Poulsen, David Sillam-Dussès, Nan Yao Su, Gaku Tokuda, Edward L. Vargo, Jessica L. Ware, Jan Šobotník, Rudolf H. Scheffrahn, Eliana Cancello, Yves Roisin, Michael S. Engel, Thomas Bourguignon

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Abstract

The higher classification of termites requires substantial revision as the Neoisoptera, the most diverse termite lineage, comprise many paraphyletic and polyphyletic higher taxa. Here, we produce an updated termite classification using genomic-scale analyses. We reconstruct phylogenies under diverse substitution models with ultraconserved elements analyzed as concatenated matrices or within the multi-species coalescence framework. Our classification is further supported by analyses controlling for rogue loci and taxa, and topological tests. We show that the Neoisoptera are composed of seven family-level monophyletic lineages, including the Heterotermitidae Froggatt, Psammotermitidae Holmgren, and Termitogetonidae Holmgren, raised from subfamilial rank. The species-rich Termitidae are composed of 18 subfamily-level monophyletic lineages, including the new subfamilies Crepititermitinae, Cylindrotermitinae, Forficulitermitinae, Neocapritermitinae, Protohamitermitinae, and Promirotermitinae; and the revived Amitermitinae Kemner, Microcerotermitinae Holmgren, and Mirocapritermitinae Kemner. Building an updated taxonomic classification on the foundation of unambiguously supported monophyletic lineages makes it highly resilient to potential destabilization caused by the future availability of novel phylogenetic markers and methods. The taxonomic stability is further guaranteed by the modularity of the new termite classification, designed to accommodate as-yet undescribed species with uncertain affinities to the herein delimited monophyletic lineages in the form of new families or subfamilies.

Original languageEnglish
Article number6724
Number of pages17
JournalNature Communications
Volume15
Issue number1
Early online date7 Aug 2024
DOIs
Publication statusE-pub ahead of print - 7 Aug 2024
Externally publishedYes

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Funder

All samples reported in this study were housed in collections, and no new field collection was performed. Specimens from collections were obtained in accordance with local and worldwide regulations at the time of their collection. Specifically, this involved the terms of the following permits: Australia, no sampling permits required; Bolivia, No. MMAyA-VMABCCGDF-DGBAP No. 1052/2013; Brazil, No. IBAMA #144/2010 and SISBIO #40673; Cameroon, No. 000000010/MINRESI/B00/C00/C10/C12 and No. 00000075/MINRESI/B00/C00/C10/C12; Democratic Republic of Congo (DRC), collections permitted under Belgian Science Policy (BELSPO) institutional project COBIMFO (2010\u20132015), as well as during the Boyekoli-Ebale-Congo Expedition in 2010 (organised by: the University of Kisangani (DRC), the Royal Museum of Central Africa (Tervuren, Belgium), the Royal Belgian Institute of Natural Sciences, the National Botanical Garden of Belgium; supported by: the Belgian Development Cooperation, BELSPO); Ecuador, No. 06-2011-FAU-DPAP-MA; French Guiana, No. TREL1902817S/136; Israel, no permits required; Ivory Coast, permits granted for protected areas (Ta\u00EF, Marahou\u00E9, Como\u00E9, Banco) by Office Ivoirien des Parcs et R\u00E9serves; Kenya, No. NACOSTI/P/15/7983/7214; Madagascar, No. 035/19/MEDD/SG/DGF/DSAP/SCB.Re and No. 202-19/MEDD/SG/DIREDD.AATS.ANS.AND; Martinique, no permits required; Mexico, permits provided to the late Paul M. Ban in 1996; Panama, No. SEX/A-36-10; Paraguay, permits provided to Rudolf Scheffrahn through the Museo Nacional de Historia Natural del Paraguay in 2012; Peru, Carta No. 592-2014-MINAGRI-DGFFS/DGEFFS; Singapore, No. NP/RP12-063a; Thailand, sampling carried out through the Khao Chong Insect Laboratory; USA, no permits required; Venezuela, permits provided to Rudolf Scheffrahn in 2008.

We thank our esteemed colleagues P. Ban, J. Cabral, J. Chase, B. Forschler, M. Hasson, R. Hickman, N. Kanzaki, P. Kasangij, J. K\u0159e\u010Dek, E. Kuswanto, B. Leru, J. Mangold, A. Mullins, T. Nishimura, R.G. Santos, R. Setter, and S. Traor\u00E9, for the collection of samples. We thank the Sequencing Section (SQC) and the Scientific Computing & Data Analysis Section (SCDA) of OIST for assistance with sequencing and providing access to the OIST computing cluster, respectively. This work was supported by the Czech Science Foundation (project No. 20-20548S to T.B.), as well as subsidiary funding from OIST to T.B., including funding for a workshop held at OIST in early December 2022 on the phylogeny and classification of termites. S.H. acknowledges the Fonds de la Recherche Scientifique \u2013 FNRS. The participation of M.S.E. was funded by CONCYTEC through the PROCIENCIA programme within the framework of the call \u201CInterinstitutional Alliances for Doctorate Programmes\u201D, according to contract PE501084299-2023-PROCIENCIA-BM.

Funding

All samples reported in this study were housed in collections, and no new field collection was performed. Specimens from collections were obtained in accordance with local and worldwide regulations at the time of their collection. Specifically, this involved the terms of the following permits: Australia, no sampling permits required; Bolivia, No. MMAyA-VMABCCGDF-DGBAP No. 1052/2013; Brazil, No. IBAMA #144/2010 and SISBIO #40673; Cameroon, No. 000000010/MINRESI/B00/C00/C10/C12 and No. 00000075/MINRESI/B00/C00/C10/C12; Democratic Republic of Congo (DRC), collections permitted under Belgian Science Policy (BELSPO) institutional project COBIMFO (2010\u20132015), as well as during the Boyekoli-Ebale-Congo Expedition in 2010 (organised by: the University of Kisangani (DRC), the Royal Museum of Central Africa (Tervuren, Belgium), the Royal Belgian Institute of Natural Sciences, the National Botanical Garden of Belgium; supported by: the Belgian Development Cooperation, BELSPO); Ecuador, No. 06-2011-FAU-DPAP-MA; French Guiana, No. TREL1902817S/136; Israel, no permits required; Ivory Coast, permits granted for protected areas (Ta\u00EF, Marahou\u00E9, Como\u00E9, Banco) by Office Ivoirien des Parcs et R\u00E9serves; Kenya, No. NACOSTI/P/15/7983/7214; Madagascar, No. 035/19/MEDD/SG/DGF/DSAP/SCB.Re and No. 202-19/MEDD/SG/DIREDD.AATS.ANS.AND; Martinique, no permits required; Mexico, permits provided to the late Paul M. Ban in 1996; Panama, No. SEX/A-36-10; Paraguay, permits provided to Rudolf Scheffrahn through the Museo Nacional de Historia Natural del Paraguay in 2012; Peru, Carta No. 592-2014-MINAGRI-DGFFS/DGEFFS; Singapore, No. NP/RP12-063a; Thailand, sampling carried out through the Khao Chong Insect Laboratory; USA, no permits required; Venezuela, permits provided to Rudolf Scheffrahn in 2008. We thank our esteemed colleagues P. Ban, J. Cabral, J. Chase, B. Forschler, M. Hasson, R. Hickman, N. Kanzaki, P. Kasangij, J. K\u0159e\u010Dek, E. Kuswanto, B. Leru, J. Mangold, A. Mullins, T. Nishimura, R.G. Santos, R. Setter, and S. Traor\u00E9, for the collection of samples. We thank the Sequencing Section (SQC) and the Scientific Computing & Data Analysis Section (SCDA) of OIST for assistance with sequencing and providing access to the OIST computing cluster, respectively. This work was supported by the Czech Science Foundation (project No. 20-20548S to T.B.), as well as subsidiary funding from OIST to T.B., including funding for a workshop held at OIST in early December 2022 on the phylogeny and classification of termites. S.H. acknowledges the Fonds de la Recherche Scientifique \u2013 FNRS. The participation of M.S.E. was funded by CONCYTEC through the PROCIENCIA programme within the framework of the call \u201CInterinstitutional Alliances for Doctorate Programmes\u201D, according to contract PE501084299-2023-PROCIENCIA-BM.

FundersFunder number
Botanic Garden Meise
Diabetes Research Connection
Belgian Federal Science Policy Office
Royal Museum for Central Africa
Koninklijk Belgisch Instituut voor Natuurwetenschappen
University of Kisangani
Okinawa Institute of Science and Technology
Fonds De La Recherche Scientifique - FNRS
Université de GuyaneTREL1902817S/136
Czech Science Foundation20-20548S
Office Ivoirien des Parcs et Réserves202-19/MEDD/SG/DIREDD, 035/19/MEDD/SG/DGF/DSAP/SCB.Re, NACOSTI/P/15/7983/7214
Belgisch Ontwikkelingsagentschap06-2011-FAU-DPAP-MA
Consejo Nacional de Ciencia, Tecnología e Innovación TecnológicaPE501084299-2023-PROCIENCIA-BM

    Keywords

    • Comparative genomics
    • Entomology
    • Phylogenomics
    • Phylogeny
    • Taxonomy

    ASJC Scopus subject areas

    • General Chemistry
    • General Biochemistry,Genetics and Molecular Biology
    • General Physics and Astronomy

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