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Type: Article
Published: 2022-12-22
Page range: 467-477
Abstract views: 237
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New Tullbergiidae mitogenomes as the evidence of sister relationship with Onychiuridae (Hexapoda, Collembola)

School of Life Sciences, East China Normal University, Shanghai 200241, China
atural History Research Center, Shanghai Natural History Museum, Shanghai Science & Technology Museum, Shanghai, 200041, China
Natural History Research Center, Shanghai Natural History Museum, Shanghai Science & Technology Museum, Shanghai, 200041, China
Natural History Research Center, Shanghai Natural History Museum, Shanghai Science & Technology Museum, Shanghai, 200041, China
School of Life Sciences, East China Normal University, Shanghai 200241, China
Collembola Onychiuroidea mitochondrial genomes phylogenetic analysis China

Abstract

Members of the order Poduromorpha are mostly small and delicate, many of them are notably smaller than 1 mm. For this reason, studies at the molecular level are still scarce, but modern sequencing technologies are making it possible and the Collembola genetic database have increased significantly in the last ten years. In order to contribute to future studies at the molecular level of the group, we sequenced and annotated three mitogenomes of Tullbergiidae species from China, two of them are newly determined. The mitogenomes of Paratullbergia changfengensis, Metaphorura motuoensis and Mesaphorura yosii have 15,210 bp, 14,873 bp and 14,831 bp in length, respectively, containing 13 protein-coding genes (PCGs), 22 transfer-RNA-coding genes (tRNA), and 2 ribosomal-RNA-coding genes (rRNA) with the ancestral Pancrustacean gene order, typical for most mitogenomes of Collembola. We performed phylogenetic analyses based on 13 PCGs with protein sequences using Bayesian inference and maximum likelihood methods. Our phylogenetic analyses including all available mitogenomes of Poduromorpha and the new mitogenomes consistently confirmed the taxonomical placement of the three Chinese species within Tullbergiidae with high support. The monophyly of the family was confirmed with Onychiuridae as its sister group.

 

References

  1. Bagnall, R.S. (1935) On the classification of the Onychiuridae (Collembola), with particular reference to the Genus Tullbergia Lubbock and its Allies. Annals & Magazine of natural History, Series 10, 15 (86), 236–242. https://doi.org/10.1080/00222933508654961
    Bagnall, R.S. (1936) The British Tullbergiinae. Part II. Entomologists Monthly Magazine, 72, 34–40.
    Bellinger, P.F., Christiansen, K.A. & Janssens, F. (1996–2022) Checklist of the Collembola of the World. Available from: http://www.collembola.org (accessed 15 October 2022)
    Börner, C. (1901) Zur Kenntnis der Apterygoten-Fauna von Bremen und der Nachbardistrikte. Beitrag zu einer Apterygoten-Fauna Mitteleuropas. Abhandlungen des Naturwissenschaftlichen Vereins zu Bremen, 17 (1), 1–141. https://doi.org/10.5962/bhl.part.18332
    Börner C. (1902) Das genus Tullbergia Lubbock. Zoologischer Anzeiger, 26, 123–131.
    Börner, C. (1903) Neue altweltliche Collembolen, nebst Bemerkungen zur Systematik der Isotominen und Entomobryinen. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin, 129–182. https://doi.org/10.5962/bhl.part.29866
    Bu, Y. & Gao, Y. (2015) Paratullbergia Womersley in China: the description of a new species and a key to the genus (Collembola, Tullbergiidae). ZooKeys, 534, 55–60. https://doi.org/10.3897/zookeys.534.6036
    Bu, Y. & Gao, Y. (2017) Study on Tullbergiidae of Tibet, China I. Metaphorura, Mesaphorura and Prabhergia (Hexapoda, Collembola). ZooKeys, 686, 85–94. https://doi.org/10.3897/zookeys.686.11468
    Bu, Y. & Gao, Y. (2019a) Study on Tullbergiidae of Tibet, China II. Metaphorura zhongi sp. n. from Sejila Mountain (Hexapoda, Collembola). Species, 20, 84–89.
    Bu, Y. & Gao, Y. (2019b) New species of Paratullbergia and Pongeiella (Collembola: Tullbergiidae) from northwest China. Entomotaxonomia, 41 (1), 64–72.
    Carapelli, A., Fanciulli, P.P.P., Frati, F. & Leo, C. (2019) Mitogenomic data to study the taxonomy of Antarctic springtail species (Hexapoda: Collembola) and their adaptation to extreme environments. Polar Biology, 42, 715–732. https://doi.org/10.1007/s00300-019-02466-8
    Carapelli, A., Greenslade, P., Nardi F., Leo, C., Convey, P., Frati, F. & Fanciulli, P.P. (2020) Evidence for cryptic diversity in the “Pan‐Antarctic” springtail Friesea antarctica and the description of two new Species. Insects, 11, 141. https://doi.org/10.3390/insects11030141
    Caroli, E. (1912) Contribuzioni alla conosenza dei Collemboli italiani. I. La tribù degli Achorutini CB. (1906). Achorutes aurantiacus n. sp., Archivio zoologico italiano, 6, 367–370.
    Carpenter, G.H. (1908) Insecta Aptera. National Antarctic Expedition, 1901–1904. Natural History, Zoology, 4, 1–5.
    Criscuolo, A. & Gribaldo, S. (2010) BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evolutionary Biology, 10 (210), 2–21. https://doi.org/10.1186/1471-2148-10-210
    Cucini, C., Fanciulli, P.P., Frati, F., Convey, P., Nardi, F. & Carapelli, A. (2021) Re‐evaluating the internal phylogenetic relationships of collembola by means of mitogenome data. Genes, 12, 1–20. https://doi.org/10.3390/genes12010044
    Deharveng, L. & Weiner, W.M. (1984) Collemboles de Corée du Nord. III–Morulinae et Neanurinae. Travaux du Laboratoire d’Écobiologie des Arthropodes Edaphiques, Toulouse, 4, 1–64.
    Denis, J.R. (1929) Notes sur les Collemboles récoltés dans ses voyages par le Prof. F. Silvestri (II), Seconde note sur les Collembola d’Extrème-Orient. Bollettino del Laboratorio di zoologia generale e agraria della Facoltà agraria in Portici, 22, 305–320.
    Denis, J.R. (1931) Contributo alla conoscenza del microgenton di Costa Rica II. Collemboles de Costa Rica avec une contribution au species de l’ordre. Bolletino del Laboratorio di Entomologia Agraria, 25, 69–170.
    Dierckxsens, N., Mardulyn, P. & Smits, G. (2016) NOVOPlasty: De novo assembly of organelle genomes from whole genome data. Nucleic Acids Research, 45 (4), e18. https://doi.org/10.1093/nar/gkw955
    Ellis, W.N. (1976) Automn fauna of Collembola from Central Crete. Tijdschrift voor Entomologie, 119, 221–326.
    Folsom, J.W. (1898) Japanese Collembola Part I. The Bulletin of the Essex Institute, 29, 51–57. https://doi.org/10.5962/bhl.part.14789
    Gao, Y. & Bu, Y. (2020) Description of a new species of Paratullbergia (Collembola, Tullbergiidae) from China with the report of an abnormal antenna. Zootaxa, 4808 (1), 121–130. https://doi.org/10.11646/zootaxa.4808.1.6
    Gao, Y. & Bu, Y. (2022) New species and records of Tullbergiidae (Collembola, Poduromorpha) from Xinjiang province, Northwest China. Zootaxa, 5092 (5), 531–544. https://doi.org/10.11646/zootaxa.5092.5.2
    Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59 (3), 307–321. https://doi.org/10.1093/sysbio/syq010
    Haas, B.J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P.D., Bowden, J., Couger, M.B., Eccles, D., Li, B., Lieber, M., Macmanes, M.D., Ott, M., Orvis, J., Pochet, N., Strozzi, F., Weeks, N., Westerman, R., William, T., Dewey, C.N., Henschel, R., Leduc, R.D., Friedman, N. & Regev, A. (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols, 8, 1494–1512. https://doi.org/10.1038/nprot.2013.084
    Jagatap, H., Monsanto, D.M., Van-Vuuren, B.J., Janion-Scheepers, C., Sekar, S., Teske, P.R. & Emami-Khoyi, A. (2019) The complete mitogenome of the springtail Tullbergia bisetosa: a subterranean springtail from the sub-Antarctic region. Mitochondrial DNA, Part B, 4 (1), 1594–1596. https://doi.org/10.1080/23802359.2019.1601514
    Hoang, D.T., Vinh, L.S., Flouri, T., Stamatakis, A., von Haeseler, A. & Minh, B.Q. (2018) MPBoot: fast phylogenetic maximum parsimony tree inference and bootstrap approximation. BMC Evolutionary Biology, 18, 1–11. https://doi.org/10.1186/s12862-018-1131-3
    Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285
    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010
    Lartillot, N., Rodrigue, N., Stubbs, D. & Richer, J. (2013) PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. Systematic Biology, 62 (4), 611–615. https://doi.org/10.1093/sysbio/syt022
    Lee, B.H. (1973) Étude de la faune Coréenne des Collemboles I. Liste des Collemboles de Corée et description de trois éspeces nouvelles. Revue d’Écologie et de Biologie du Sol, 10 (3), 435–449.
    Leo, C., Carapelli, A., Cicconardi, F., Frati, F. & Nardi, F. (2019) Mitochondrial genome diversity in Collembola: Phylogeny, dating and gene order. Diversity, 11, 1–20. https://doi.org/10.3390/d11090169
    Linnaeus, C. (1758) Systema Naturae per Regna tria Naturae, secundum classes, ordines, genera, species, cumcharacteribus, differentiis, synonymis, locis. Tomus 1. Editio Decima. Laurentii Salvii, Holmiae, 823 pp. https://doi.org/10.5962/bhl.title.542
    Meng, G., Li, Y., Yang, C. & Liu, S. (2019) MitoZ: A toolkit for animal mitochondrial genome assembly, annotation and visualization. Nucleic Acids Research, 47 (11), e63. https://doi.org/10.1093/nar/gkz173
    Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., von Haeseler, A. & Lanfear, R. (2020) IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular biology and evolution, 37, 1530–1534. https://doi.org/10.1093/molbev/msaa015
    Nardi, F., Carapelli, A., Fanciulli, P.P., Dallai, R. & Frati, F. (2001) The complete mitochondrial DNA sequence of the basal hexapod Tetrodontophora bielanensis: Evidence for heteroplasmy and tRNA translocations. Molecular Biology and Evolution, 18, 1293–1304. https://doi.org/10.1093/oxfordjournals.molbev.a003914
    Rambaut, A. (2010) FigTree. Version 1.3.1. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. Available from: http://tree.bio.ed.ac.uk/software/figtree/ (accessed 5 December 2022)
    Rusek, J. (1967) Beitrag zur Kenntnis der Collembola (Apterygota) Chinas. Acta Entomologica Bohemoslovaca, 64, 184–194.
    Rusek, J. (1976) New Onychiuridae (Collembola) from Vancouver Island. Canadian Journal of Zoology, 54, 19–41. https://doi.org/10.1139/z76-003
    Rusek, J. (1982) Multivesicula gen. n. from the subfamily Tullbergiinae (Collembola: Onychiuridae). Věstník Československé společnosti Zoologické, 46, 33–44.
    Schäffer, C. (1891) Die Collembolen von Süd-Georgien. Nach der Ausbeute der deutschen station von 1882/83. Jahrbuch der Hamburgischen Wissenschaftlichen Anstalten, 9, 3–10.
    Schäffer, C. (1896) Die Collembola der Umgebung von Hamburg und benachbarter Gebiete. Jahrbuch der Hamburgischen Wissenschaftlichen Anstalten, 13, 149–220.
    Schäffer, C. (1900) Ueber württembergische Collembola. Jahreshefte des Vereins für Vaterländische Naturkunde in Württemberg, 56, 245–280.
    Stach, J. (1964) Materials to the knowledge of Chinese collembolan fauna. Acta zoologica cracoviensia, 6, 1–26.
    Steenwyk, J.L., Buida, T.J., Labella, A.L., Li, Y., Shen, X.X. & Rokas, A. (2021) PhyKIT: a broadly applicable UNIX shell toolkit for processing and analyzing phylogenomic data. Bioinformatics, 1, 7. https://doi.org/10.1093/bioinformatics/btab096
    Sun, X., Ding, Y., Orr, M.C. & Zhang, F. (2020a) Streamlining universal single-copy orthologue and ultraconserved element design: A case study in Collembola. Molecular Ecology Resources, 20, 706–717. https://doi.org/10.1111/1755-0998.13146
    Sun, X., Yu, D., Xie, Z., Dong, J., Ding, Y., Yao, H., Greenslade, P., Id, D.Y., Xie, Z., Dong, J., Ding, Y., Yao, H. & Greenslade, P. (2020b) Phylomitogenomic analyses on collembolan higher taxa with enhanced taxon sampling and discussion on method selection. PloS ONE, 15, 1–21. https://doi.org/10.1371/journal.pone.0230827
    Waga, A. (1842) Description d’un insecte aptère qui se trouve en quantité aux environs de Varsovie. Annales de la Société Entomologique de France, 11, 264–272.
    Wahlgren, E. (1906) Antarktische und Subantarktische Collembolen gesammelt von der Schwedischen Südpolarexpedition. Wissenschaftliche Ergebnisse der Schwedischen Südpolarexpedition, 5 (9), 1–22.
    Willem, V. (1901) Les Collemboles recueillis par l’expédition Antarctique Belge. Annales de la Société Entomologiquede Belgique, 45, 260–262.
    Womersley, H. (1930) Some additions to the Collembola of Britain. Annals and Magazine of Natural History, Series 10, 6 (31), 149–153. https://doi.org/10.1080/00222933008673197

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