Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2020-04-23
Page range: 56–70
Abstract views: 144
PDF downloaded: 5

Distribution of Macrobiotus shonaicus Stec, Arakawa & Michalczyk, 2018 (Tardigrada: Eutardigrada: Macrobiotidae) in Japan

School of Fundamental Science and Technology, Graduate School of Science and Technology, Keio University
Institute for Advanced Biosciences, Keio University, Japan gaou@sfc.keio.ac.jp https://orcid.org/0000-0002-2893-4919 Faculty of Environment and Information Studies, Keio University, Japan Exploratory Research Center on Life and Living Systems, National Institutes of Natural Sciences, 5-1 Higashiyama, Myodaiji, Okazaki 444-8787, Japan
Exploratory Research Center on Life and Living Systems, National Institutes of Natural Sciences, 5-1 Higashiyama, Myodaiji, Okazaki 444-8787, Japan Department of Biosciences and Informatics, Faculty of Science and Technology, Keio University, 3-14-1 Hiyoshi, Kohoku, Yokohama, Kanagawa, Japan
Tardigrada DNA barcoding geographic distribution karyotype mating tardigrade

Abstract

To date, only seven species of Macrobiotidae (Parachela; Eutardigrada; Tardigrada) have been reported from Japan, including the recently described Macrobiotus shonaicus Stec et al., 2018 from the Shonai region of Japan. This species has flexible filaments on the egg processes and is known to proliferate only through sexual reproduction. Here, we report a multifaceted analysis of nine populations of M. shonaicus found on four Japanese islands. DNA sequencing of the cytochrome oxidase subunit I (COI) and internal transcribed spacer 2 (ITS-2) of the nine populations revealed 8 and 11 haplotypes, respectively. The extensive morphometric analysis showed considerably greater variability in the morphology of eggs than of animals. In addition to the morphological and molecular data, we confirmed the karyotype and found that all populations had a chromosome number of n = 6. Moreover, we observed and filmed mating behaviour between all studied populations of M. shonaicus. Our results clearly indicated that M. shonaicus is widely distributed throughout Japan.

 

References

  1. Arakawa, K., Yoshida, Y. & Tomita, M. (2016) Genome sequencing of a single tardigrade Hypsibius dujardini individual. Scientific Data, 3, 160063.

    https://doi.org/10.1038/sdata.2016.63

    Bertolani, R. & Rebecchi, L. (1993) A revision of the Macrobiotus hufelandi group (Tardigrada, Macrobiotidae), with some observations on the taxonomic characters of eutardigrades. Zoologica scripta, 22 (2), 127–152.

    https://doi.org/10.1111/j.1463-6409.1993.tb00347.x

    Bertolani, R., Rebecchi, L., Giovannini, I. & Cesari, M. (2011) DNA barcoding and integrative taxonomy of Macrobiotus hufelandi C.A.S. Schultze 1834, the first tardigrade species to be described, and some related species. Zootaxa, 2997 (1), 19–36.

    https://doi.org/10.11646/zootaxa.2997.1.2

    Bertolani, R., Guidetti, R., Marchiro, T., Altiero, T., Rebecchi, L. & Cesari, M. (2014) Phylogeny of Eutardigrada: New molecular data and their morphological support lead to the identification of new evolutionary lineages. Molecular Phylogenetics and Evolution, 76, 110–126.

    https://doi.org/10.1016/j.ympev.2014.03.006

    Biserov, V.I., Dudichev, A.L. & Biserova, N.M. (2001) Preliminary data on tardigrades of Lake Biwa (Japan). Arthropoda Selecta, 10, 307–310.

    Cesari, M.., Bertolani, R., Rebecchi, L. & Guidetti, R. (2009) DNA barcoding in Tardigrada: the first case study on Macrobiotus macrocalix Bertolani & Rebecchi 1993 (Eutardigrada, Macrobiotidae). Molecular Ecology Resources, 9 (3), 699–706.

    https://doi.org/10.1111/j.1755-0998.2009.02538.x

    Cesari, M., Giovanni, I., Bertolani, R. & Rebecchi, L. (2011) An example of problems associated with DNA barcoding in tardigrades: a novel method for obtaining voucher specimens. Zootaxa, 3104, 42–51

    https://doi.org/10.11646/zootaxa.3104.1.3

    Clement, M., Snell, Q., Walker, P., Posada, D. & Crandall, K. (2002) TCS: Estimating gene genealogies. 16th International Parallel and Distributed Processing Symposium. International Proceedings. 2, 184.

    https:// doi.org/10.1109/ipdps.2002.1016585

    Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular marine biology and biotechnology, 3, 294–99.

    Guidetti, R., Gandolfi, A., Rossi, V. & Bertolani, R. (2005) Phylogenetic analysis of Macrobiotidae (Eutardigrada, Parachela): a combined morphological and molecular approach. Zoologica Scripta, 34, 235–244.

    https://doi.org/10.1111/j.1463-6409.2005.00193.x

    Guidetti, R., Peluffo, J.R., Rocha, A.M., Cesari, M. & Moly de Peluffo, M.C. (2013) The morphological and molecular analyses of a new South American urban tardigrade offer new insights on the biological meaning of the Macrobiotus hufelandi group of species (Tardigrada: Macrobiotidae). Journal of Natural History, 47 (37–38), 2409–2426.

    https://doi.org/10.1080/00222933.2013.800610

    Guidetti, R., Cesari, M., Bertolani, R., Altiero, T. & Rebecchi, L. (2019) High diversity in species, reproductive modes and distribution within the Paramacrobiotus richtersi complex (Eutardigrada, Macrobiotidae). Zoological letters, 5 (1), 1–28.

    https://doi.org/10.1186/s40851-018-0113-z

    Guidi, A. & Rebecchi, L. (1996) Spermatozoan morphology as a character for tardigrade systematics: comparison with sclerified parts of animals and eggs in eutardigrades. Zoological Journal of the Linnean Society, 116, 101–113.

    https://doi.org/10.1006/zjls.1996.0009

    Hatai, S. (1956) On the Japanese Tardigrada. Science Report Of The Yokosuka City Museum, 1, 1–13.

    Ishida, M. & Matsui, T. (2007) Noteworthy tardigrades from Kochi Prefecture. The Natural Environmental Scientific Research, 9, 45–58. [In Japanese, with English summary]

    Ito, M. (1997) Taxonomic study on the Eutardigrada from the northern slope of Mt. Fuji, central Japan. III. Families Macrobiotidae and Milnesiidae. Species Diversity, 2, 167–178.

    https://doi.org/10.12782/specdiv.2.167

    Ito, M. (1999) Ecological distribution, abundance and habitat preference of terrestrial tardigrades in various forests on the northern slope of Mt. Fuji, central Japan. Zoologischer Anzeiger, 238, 225–234.

    Kaczmarek, Ł. & Michalczyk, Ł. (2017) The Macrobiotus hufelandi group (Tardigrada) revisited. Zootaxa, 4363 (1), 101–113.

    https://doi.org/10.11646/zootaxa.4363.1.4

    Katoh, K., Misawa, K., Kuma, K. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059–66.

    https://doi.org/10.1093/nar/gkf436

    Katoh, K. & Toh, H. (2008) Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics, 9, 286–98.

    https://doi.org/10.1093/bib/bbn013

    Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.

    https://doi.org/10.1093/molbev/msw054

    Lanfear, R., Hua, X. & Warren, D.L. (2016) Estimating the effective sample size of tree topologies from Bayesian phylogenetic analyses. Genome Biology and Evolution, 8, 2319–2332.

    https://doi.org/10.1093/gbe/evw171

    Leigh, J.W. & Bryant, D. (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6, 1110–1116.

    https://doi.org/10.1111/2041-210X.12410

    Mathews, G. (1937) Tardigrada from Japan. Peking Natural History Bulletin, 11, 411–412.

    Morek, W., Gąsiorek, P., Stec, D., Bladgen, B. & Michalczyk, Ł. (2016) Experimental taxonomy exposes ontogenetic variability and elucidates the taxonomic value of claw configuration in Milnesium Doyère, 1840 (Tardigrada: Eutardigrada: Apochela). Contributions to Zoology, 85 (2), 173–200.

    https://doi.org/10.1163/18759866-08502003

    Morek, W. & Michalczyk, Ł. (2020) First extensive multilocus phylogeny of the genus Milnesium (Tardigrada) reveals no congruence between genetic markers and morphological traits. Zoological Journal of the Linnean Society, 188 (3), 681–693.

    https://doi.org/10.1093/zoolinnean/zlz040

    Morek, W., Stec, D., Gąsiorek, P., Surmacz, B. & Michalczyk, Ł. (2019a) Milnesium tardigradum Doyère, 1840: The first integrative study of interpopulation variability in a tardigrade species. Journal of Zoological Systematics and Evolutionary Research, 2018, 1–23.

    https://doi.org/10.1111/jzs.12233

    Morek, W., Suzuki, A.C., Schill, R.O., Georgiev, D., Yankova, M., Marley N.J. & Michalczyk, Ł. (2019b) Redescription of Milnesium alpigenum Ehrenberg, 1853 (Tardigrada: Apochela) and a description of Milnesium inceptum sp. nov., a tardigrade laboratory model. Zootaxa, 4586 (1), 35–64.

    https://doi.org/10.11646/zootaxa.4586.1.2

    Nowak, B. & Stec, D. (2018) An integrative description of Macrobiotus hannae sp. nov. (Tardigrada: Eutardigrada: Macrobiotidae: hufelandi group) from Poland. Turkish Journal of Zoology, 42, 269–286.

    https://doi.org/10.3906/zoo-1712-31

    Pilato, G. (1981) Analisi di nuovi caratteri nello studio degli Eutardigradi. Animalia, 8, 51–57.

    R Core Team. (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: https://www.R-project.org (accessed 5 April 2016)

    Rebecchi, L. & Guidi A. (1991) First SEM studies on tardigrade spermatozoa. Invertebrate Reproduction and Development, 19 (2), 151–156.

    https://doi.org/10.1080/07924259.1991.9672169

    Rebecchi, L. (1997) Ultrastructural Study of Spermiogenesis and the Testicular and Spermathecal Spermatozoon of the Gonochoristic Tardigrade Xerobiotus pseudohufelandi (Eutardigrada, Macrobiotidae). Journal of Morphology, 234, 11–24.

    https://doi.org/10.1002/(SICI)1097-4687(199710)234:1<11::AID-JMOR2>3.0.CO;2-Q

    Rebecchi, L. (2001) The spermatozoon in Tardigrades: Evolution and Relationships with the Environment*. Zoologisher Anzeiger, 240, 525–533.

    https://doi.org/10.1078/0044-5231-00063

    Rebecchi, L., Altiero, L. & Guidi, A. (2011) The ultrastructure of the tardigrade spermatozoon: a comparison between Paramacrobiotus and Macrobiotus species (Eutardigrada). Invertebrate Zoology, 8 (1), 63–77.

    https://doi.org/10.15298/invertzool.08.1.08

    Ronquist, F. & Huelsenbeck, J.P. (2012) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–4.

    https://doi.org/10.1093/bioinformatics/btg180

    Roszkowska, M., Ostrowska, M., Stec, D., Janko, K. & Kaczmarek, Ł. (2017) Macrobiotus polypiformis sp. nov., a new tardigrade (Macrobiotidae; hufelandi group) from the Ecuadorian Pacific coast, with remarks on the claw abnormalities in eutardigrades. European Journal of Taxonomy, 327, 1–19.

    https://doi.org/10.5852/ejt.2017.327

    Schill, R.O., Forster, F., Dandekar, T. & Wolf, N. (2010) Using compensatory base change analysis of internal transcribed spacer 2 secondary structures to identify three new species in Paramacrobiotus (Tardigrada). Organisms Diversity & Evolution, 10 (4), 287–296.

    https://doi.org/10.1007/s13127-010-0025-z

    Stamatakis, A. (2014) RaxML version 8: A tool for phylogenetic analysis and post‐analysis of large phylogenies. Bioinformatics, 30, 1312–1313.

    https://doi.org/10.1093/bioinformatics/btu033

    Stec, D., Smolak, R., Kaczmarek, Ł. & Michalczyk, Ł. (2015) An integrative description of Macrobiotus paulinae sp. nov. (Tardigrada: Eutardigrada: Macrobiotidae: hufelandi group) from Kenya. Zootaxa, 4052 (5), 501–526.

    https://doi.org/10.11646/zootaxa.4052.5.1

    Stec, D., Morek, W., Gąsiorek, P., Kaczmarek, Ł. & Michalczyk, Ł. (2016) Determinants and taxonomic consequences of extreme egg shell variability in Ramazzottius subanomalus (Biserov, 1985) (Tardigrada). Zootaxa, 4208 (2), 176–188.

    https://doi.org/10.11646/zootaxa.4208.2.5

    Stec, D., Morek, W., Gąsiorek, P., Blagden, B. & Michalczyk, Ł. (2017) Description of Macrobiotus scoticus sp. nov. (Tardigrada: Macrobiotidae: hufelandi group) from Scotland by means of integrative taxonomy. Annales Zoologici, 67 (2), 181–197.

    https://doi.org/10.3161/00034541ANZ2017.67.2.001

    Stec, D., Arakawa, K. & Michalczyk, Ł. (2018a) An integrative description of Macrobiotus shonaicus sp. nov. (Tardigrada: Macrobiotidae) from Japan with notes on its phylogenetic position within the hufelandi group. PloS One, 13 (2), e0192210.

    https://doi.org/10.1371/journal.pone.0192210

    Stec, D., Kristensen, R.M. & Michalczyk, Ł. (2018b) Integrative taxonomy identifies Macrobiotus papei, a new tardigrade species of the hufelandi complex (Eutardigrada: Macrobiotidae) from the Udzungwa Mountains National Park (Tanzania). Zootaxa, 4446 (2), 273–291.

    https://doi.org/10.11646/zootaxa.4446.2.7

    Stec, D., Morek, W., Gąsiorek, P. & Michalczyk, Ł. (2018c) Unmasking hidden species diversity within the Ramazzottius oberhaeuseri complex, with an integrative redescription of the nominal species for the family Ramazzottiidae (Tardigrada: Eutardigrada: Parachela) Systematics and Biodiversity, 16 (4), 357–376.

    https://doi.org/10.1080/14772000.2018.1424267

    Stec, D., Krzywański, Ł. & Michalczyk, Ł. (2018d) Integrative description of Macrobiotus canaricus sp. nov. with notes on M. recens (Eutardigrada: Macrobiotidae). European Journal of Taxonomy, 452, 1–36.

    https://doi.org/10.5852/ejt.2018.452

    Stec, D., Krzywański, Ł., Zawierucha, K. & Michalczyk, Ł. (2020) Untangling systematics of the Paramacrobiotus areolatus species complex by an integrative redescription of the nominal species for the group, with multilocus phylogeny and species delineation within the genus Paramacrobiotus. Zoological Journal of the Linnean Society, 188 (3), 694–716.

    https://doi.org/10.1093/zoolinnean/zlz163

    Sugiura, K., Minato, H., Suzuki, A.C., Arakawa, K., Kunieda, T. & Matsumoto, M. (2019) Comparison of Sexual Reproductive Behaviors in Two Species of Macrobiotidae (Tardigrada: Eutardigrada). Zoological Science, 36 (2), 120–127.

    https://doi.org/10.2108/zs180103

    Suzuki, A.C. (2017) Tardigrade Research in Japan. In: Morikawa, M. & Kajihara, H. (Eds.), Species Diversity of Animals in Japan. Springer Japan, Tokyo, pp. 267–84.

    https://doi.org/10.1007/978-4-431-56432-4_10

    Suzuki, A.C., Heard, L. & Sugiura, K. (2018) Terrestrial tardigrades from Mikurajima Island (the first report). Mikurensis, 7, 3–8.

    Utsugi, K. (1986) Urban tardigrades in Kyushu. Zoological Science, 3, 1110.

    Utsugi, K. (1987) Urban tardigrades in Hokuriku area. Zoological Science, 4, 1111.

    Utsugi, K. (1988) Tardigrades in Hokkaido area. Zoological Science, 5, 1335.

    Utsugi, K. (1995) Terrestrial tardigrades from mountain areas of Japan. Zoological science, 12 (Supplement), 36.

    Utsugi, K. (1996) Study on terrestrial tardigrades in Japan. II. Summary of urban tardigrades in Japan. The Natural Environmental Scientific Research, 9, 33–46. [in Japanese, with English summary]

    Utsugi, K., Hiraoka, T. & Nunomura, N. (1997) On the relation between tardigrade fauna and bryophyte flora in Toyama Prefecture. Bulletin of the Toyama Science Museum, 20, 57–71. [in Japanese, with English summary]

    Wełnicz, W., Grohme, M.A., Kaczmarek, Ł., Schill, R.O. & Frohme, M. (2011) ITS-2 and 18S rRNA data from Macrobiotus polonicus and Milnesium tardigradum (Eutardigrada, Tardigrada). Journal of Zoological Systematics and Evolutionary Research, 49 (Supplement 1), 34–39.

    https://doi.org/10.1111/j.1439-0469.2010.00595.x

    Wessel, P., Luis, J.F., Uieda, L., Scharroo, R., Wobbe, F., Smith, W.H.F. & Tian, D. (2019) The Generic Mapping Tools version 6. Geochemistry, Geophysics, Geosystems, 20, 5556–5564.

    https://doi.org/10.1029/2019GC008515

    White, T.J., Bruns, T., Lee, S., & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innes, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds.), PCR protocols: a guide to methods and application. Academic Press, San Diego, California, pp. 315–322.

    https://doi.org/10.1016/B978-0-12-372180-8.50042-1

    Zawierucha, Z., Stec, D., Lachowska-Cierlik, D., Takeuchi, N., Li, Z. & Michalczyk, Ł. (2018) High mitochondrial diversity in a new water bear species (Tardigrada: Eutardigrada) from mountain glaciers in central Asia, with the erection of a new genus Cryoconicus. Annales Zoologici, 68 (1), 179–201.

    https://doi.org/10.3161/00034541ANZ2018.68.1.007

    Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29, 2869–2876.

    https://doi.org/10.1093/bioinformatics/btt499