Integrative redescription of Hypsibius pallidoides Pilato et al., 2011 (Eutardigrada: Hypsibioidea) with the erection of a new genus and discussion on the phylogeny of Hypsibiidae

  • Denis V. Tumanov Department of Invertebrate Zoology, Faculty of Biology, Saint-Petersburg State University, 199034, Universitetskaya nab. 7/9, Saint Petersburg http://orcid.org/0000-0002-4190-4175
DOI: https://doi.org/10.5852/ejt.2020.681
Keywords: Tardigrada, morphology, trait evolution, Pilatobiinae, molecular taxonomy

Abstract

An integrative redescription of Hypsibius pallidoides Pilato, Kiosya, Lisi, Inshina & Biserov, 2011 was undertaken following a reexamination of the type material and new material using high-quality light microscopy, scanning electron microscopy and methods of molecular taxonomy. Detailed morphological investigations revealed a unique complex of characters that precluded the attribution of this species to the genus Hypsibius Ehrenberg, 1848. Furthermore, phylogenetic analyses indicated the affinity of this species within the subfamily Pilatobiinae (Hypsibiidae). Notahypsibius gen. nov. is erected for H. pallidoides and two putatively related species: H. scaber Maucci, 1987 and Ramazzottius arcticus (Murray, 1907). An emended diagnosis for the genus Pilatobius is given, while the subfamily Pilatobiinae lacks a cohesive morphological diagnosis despite representing, at the same time, a well-supported molecular clade. Obvious controversy between the results of the morphological and molecular analyses of the phylogeny of Hypsibioidea is discussed. The distribution of morphological characters such as the claw type, organization of the bucco-pharyngeal apparatus, and egg shell sculpture type within Eutardigrada is analyzed and their phylogenetic significance discussed.

References

Bartels P.J., Apodaca J.J., Mora C. & Nelson D.R. 2016. A global biodiversity estimate of a poorly known taxon: phylum Tardigrada. Zoological Journal of the Linnean Society 178 (4): 730–736. https://doi.org/10.1111/zoj.12441

Beasley C.W., Kaczmarek Ł. & Michalczyk Ł. 2008. Doryphoribius mexicanus, a new species of Tardigrada (Eutardigrada: Hypsibiidae) from Mexico (North America). Proceedings of the Biological Society of Washington 121 (1): 34–40. https://doi.org/10.2988/07-30.1

Bertolani R., Rebecchi L. & Claxton S.K. 1996. Phylogenetic significance of egg shell variation in tardigrades. Zoological Journal of the Linnean Society 116 (1–2): 139–148. https://doi.org/10.1111/j.1096-3642.1996.tb02339.x

Bertolani R., Biserov V., Rebecchi L. & Cesari M. 2011a. Taxonomy and biogeography of tardigrades using an integrated approach: new results on species of the Macrobiotus hufelandi group. Invertebrate Zoology 8 (1): 23–36. https://doi.org/10.15298/invertzool.08.1.05

Bertolani R., Rebecchi L., Giovannini I. & Cesari M. 2011b. 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., Marchioro 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

Binda M.G. & Kristensen R.M. 1986. Notes on the genus Oreella (Oreellidae) and the systematic position of Carphania fluviatilis Binda, 1978. (Carphaniidae fam. nov., Heterotardigrada). Animalia 13 (1/3): 9–20.

Binda M.G. & Pilato G. 1986. Ramazzottius, nuova genere di Eutardigrado (Hypsibiidae). Animalia 13 (1/3): 159–166.

Buda J., Olszanowski Z., Wierzgoń M. & Zawierucha K. 2018. Tardigrades and oribatid mites in bryo-phytes from geothermally active lava fields (Krafla, Iceland) and the description of Pilatobius islandicus sp. nov. (Eutardigrada). Polish Polar Research 39 (3): 425–453. https://doi.org/10.24425/118755

Cesari M., Vecchi M., Palmer A., Bertolani R., Pilato G., Rebecchi L. & Guidetti R. 2016. What if the claws are reduced? Morphological and molecular phylogenetic relationships of the genus Haplomacrobiotus May, 1948 (Eutardigrada, Parachela). Zoological Journal of the Linnean Society 178 (4): 819–827. https://doi.org/10.1111/zoj.12424

Cohen B.L. 2018. Match and mismatch of morphological and molecular phylogenies: causes, implications, and new light on cladistics. Zoological Journal of the Linnean Society 184 (2): 516–527. https://doi.org/10.1093/zoolinnean/zly004

Dabert M., Dastych H., Hohberg K. & Dabert J. 2014. Phylogenetic position of the enigmatic clawless eutardigrade genus Apodibius Dastych, 1983 (Tardigrada), based on 18S and 28S rRNA sequence data from its type species A. confusus. Molecular Phylogenetics and Evolution 70: 70–75. https://doi.org/10.1016/j.ympev.2013.09.012

Darriba D., Taboada G.L., Doallo R. & Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9 (8): 772. https://doi.org/10.1038/nmeth.2109

Dastych H. 1984. The Tardigrada from Antarctic with descriptions of several new species. Acta Zoologica Cracoviensia 27 (19): 377–436.

Dastych H. 1988. The Tardigrada of Poland. Wyd. 1. Państwowe Wydawn. Nauk, Warszawa.

Dastych H. 1991. Redescription of Hypsibius antarcticus (Richters, 1904), with some notes on Hypsibius arcticus (Murray, 1907) (Tardigrada). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 88: 141–159.

Dastych H. 2009. Thalerius konradi gen. nov., sp. nov., a new tardigrade from the periglacial area of the Ötztal Alps, Austria (Tardigrada). Contributions to Natural History (12): 391–402.

Dastych H. 2011. Bergtrollus dzimbowski gen. n., sp. n., a remarkable new tardigrade genus and species from the nival zone of the Lyngen Alps, Norway (Tardigrada: Milnesiidae). Entomologische Mitteilungen aus dem Zoologischen Museum Hamburg 15 (186): 335–359.

Dastych H. 2018. Redescription and revalidation of the sub-antarctic tardigrade Hypsibius murrayi (Richters, 1907) based on the rediscovered type material (Tardigrada, Panarthropoda). Entomologie heute 30: 95–115.

Dastych H. 2019. Cryobiotus roswithae gen. n., sp. n., a new genus and species of glacier-dwelling tardigrades from Northern Norway (Tardigrada, Panarthropoda). Entomologie heute 31: 95–111.

Dastych H., McInnes S.J. & Claxton S.K. 1998. Oreella mollis Murray, 1910 (Tardigrada): a redescription and revision of Oreella. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 95: 89–113.

Degma P., Bertolani R. & Guidetti R. 2019. Actual checklist of Tardigrada. 36th Edition: 1-09-2019. https://doi.org/10.25431/11380_1178608

Edgar R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32 (5): 1792–1797. https://doi.org/10.1093/nar/gkh340

Eibye-Jacobsen J. 1997. New observations on the embryology of the Tardigrada. Zoologischer Anzeiger 235: 201–216.

Eibye-Jacobsen J. 2001. A new method for making SEM preparations of the tardigrade buccopharyngeal apparatus. Zoologischer Anzeiger 240 (3–4): 309–319. https://doi.org/10.1078/0044-5231-00038

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 (5): 294–299.

Gąsiorek P. & Michalczyk Ł. 2020. Phylogeny of Itaquasconinae in the light of the evolution of the flexible pharyngeal tube in Tardigrada. Zoologica Scripta 49 (4): 499–515. https://doi.org/10.1111/zsc.12424

Gąsiorek P., Stec D., Morek W., Zawierucha K., Kaczmarek Ł., Lachowska-Cierlik D. & Michalczyk Ł. 2016. An integrative revision of Mesocrista Pilato, 1987 (Tardigrada: Eutardigrada: Hypsibiidae). Journal of Natural History 50 (45–46): 2803–2828. https://doi.org/10.1080/00222933.2016.1234654

Gąsiorek P., Zawierucha K., Stec D. & Michalczyk Ł. 2017. Integrative redescription of a common Arctic water bear Pilatobius recamieri (Richters, 1911). Polar Biology 40 (11): 2239–2252. https://doi.org/10.1007/s00300-017-2137-9

Gąsiorek P., Stec D., Morek W. & Michalczyk Ł. 2018. An integrative redescription of Hypsibius dujardini (Doyère, 1840), the nominal taxon for Hypsibioidea (Tardigrada: Eutardigrada). Zootaxa 4415 (1): 45. https://doi.org/10.11646/zootaxa.4415.1.2

Gąsiorek P., Morek W., Stec D., Blagden B. & Michalczyk Ł. 2019a. Revisiting Calohypsibiidae and Microhypsibiidae: Fractonotus Pilato, 1998 and its phylogenetic position within Isohypsibiidae (Eutardigrada: Parachela). Zoosystema 41 (1): 71–89. https://doi.org/10.5252/zoosystema2019v41a6

Gąsiorek P., Morek W., Stec D. & Michalczyk Ł. 2019b. Untangling the Echiniscus Gordian knot: paraphyly of the “ arctomys group” (Heterotardigrada: Echiniscidae). Cladistics 35: 633–653. https://doi.org/10.1111/cla.12377

Gąsiorek P., Stec D., Morek W. & Michalczyk Ł. 2019c. Deceptive conservatism of claws: distinct phyletic lineages concealed within Isohypsibioidea (Eutardigrada) revealed by molecular and morphological evidence. Contributions to Zoology 88 (1): 78–132. https://doi.org/10.1163/18759866-20191350

Gouy M., Guindon S. & Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27 (2): 221–224. https://doi.org/10.1093/molbev/msp259

Guidetti R. & Bertolani R. 2001. The tardigrades of Emilia (Italy). III. Piane di Mocogno (Northern Apennines). Zoologischer Anzeiger 240 (3): 377–383. https://doi.org/10.1078/0044-5231-00045

Guidetti R. & Pilato G. 2003. Revision of the genus Pseudodiphascon (Tardigrada, Macrobiotidae), with the erection of three new genera. Journal of Natural History 37 (14): 1679–1690. https://doi.org/10.1080/00222930210126659

Guidetti R., Nelson D.R. & Bertolani R. 1999. Ecological and faunistic studies on tardigrades in leaf litter of beach forests. Zoologischer Anzeiger 238: 215–223.

Guidetti R., Altiero T. & Hansen J.G. 2006. A new species of freshwater tardigrades from Disko Island (Greenland) increases an unsolved paradox in tardigrade systematics. Hydrobiologia 558 (1): 69–79. https://doi.org/10.1007/s10750-005-1408-6

Guidetti R., Bertolani R. & Degma P. 2007. New taxonomic position of several Macrobiotus species (Eutardigrada: Macrobiotidae). Zootaxa 1471: 61–68. https://doi.org/10.11646/zootaxa.1471.1.6

Guidetti R., Schill R.O., Bertolani R., Dandekar T. & Wolf M. 2009. New molecular data for tardigrade phylogeny, with the erection of Paramacrobiotus gen. nov. Journal of Zoological Systematics and Evolutionary Research 47 (4): 315–321. https://doi.org/10.1111/j.1439-0469.2009.00526.x

Guidetti R., Rebecchi L., Bertolani R., Jönsson K.I., Kristensen R.M. & Cesari M. 2016. Morphological and molecular analyses on Richtersius (Eutardigrada) diversity reveal its new systematic position and lead to the establishment of a new genus and a new family within Macrobiotoidea. Zoological Journal of the Linnean Society 178 (4): 834–845. https://doi.org/10.1111/zoj.12428

Guidetti R., Cesari M., Bertolani R., Altiero T. & Rebecchi L. 2019a. High diversity in species, reproductive modes and distribution within the Paramacrobiotus richtersi complex (Eutardigrada, Macrobiotidae). Zoological Letters 5 (1): 1. https://doi.org/10.1186/s40851-018-0113-z

Guidetti R., Massa E., Bertolani R., Rebecchi L. & Cesari M. 2019b. Increasing knowledge of Antarctic biodiversity: new endemic taxa of tardigrades (Eutardigrada; Ramazzottiidae) and their evolutionary relationships. Systematics and Biodiversity 17: 573–593. https://doi.org/10.1080/14772000.2019.1649737

Guil N. & Giribet G. 2012. A comprehensive molecular phylogeny of tardigrades-adding genes and taxa to a poorly resolved phylum-level phylogeny. Cladistics 28 (1): 21–49. https://doi.org/10.1111/j.1096-0031.2011.00364.x

Guil N., Machordom A. & Guidetti R. 2013. High level of phenotypic homoplasy amongst eutardigrades (Tardigrada) based on morphological and total evidence phylogenetic analyses. Zoological Journal of the Linnean Society 169 (1): 1–26. https://doi.org/10.1111/zoj.12046

Guil N., Jørgensen A. & Kristensen R. 2019. An upgraded comprehensive multilocus phylogeny of the Tardigrada tree of life. Zoologica Scripta 48 (1): 120–137. https://doi.org/10.1111/zsc.12321

Hansen J.G., Kristensen R.M., Bertolani R. & Guidetti R. 2017. Comparative analyses of Bertolanius species (Eohypsibiidae; Eutardigrada) with the description of Bertolanius birnae sp. nov. from northern polar regions. Polar Biology 40 (1): 123–140. https://doi.org/10.1007/s00300-016-1931-0

Hedges S.B. & Sibley C.G. 1994. Molecules vs. morphology in avian evolution: the case of the “pelecaniform” birds. Proceedings of the National Academy of Sciences of the United States of America 91 (21): 9861–9865. https://doi.org/10.1073/pnas.91.21.9861

Hillis D.M. 1987. Molecular versus morphological approaches to systematics. Annual Review of Ecology and Systematics 18 (1): 23–42. https://doi.org/10.1146/annurev.es.18.110187.000323

Horning D.S.J., Schuster R.O. & Grigarick A.A. 1978. Tardigrada of New Zealand. New Zealand Journal of Zoology 5 (2): 185–280. https://doi.org/10.1080/03014223.1978.10428316

Janelt K., Jezierska M. & Poprawa I. 2019. The female reproductive system and oogenesis in Thulinius ruffoi (Tardigrada, Eutardigrada, Isohypsibiidae). Arthropod Structure & Development 50: 53–63. https://doi.org/10.1016/j.asd.2019.04.003

Jørgensen A., Faurby S., Hansen J.G., Møbjerg N. & Kristensen R.M. 2010. Molecular phylogeny of Arthrotardigrada (Tardigrada). Molecular Phylogenetics and Evolution 54 (3): 1006–1015. https://doi.org/10.1016/j.ympev.2009.10.006

Jørgensen A., Møbjerg N. & Kristensen R.M. 2011. Phylogeny and evolution of the Echiniscidae (Echiniscoidea, Tardigrada) - an investigation of the congruence between molecules and morphology. Journal of Zoological Systematics and Evolutionary Research 49: 6–16. https://doi.org/10.1111/j.1439-0469.2010.00592.x

Kaczmarek Ł. & Michalczyk Ł. 2017. The Macrobiotus hufelandi group (Tardigrada) revisited. Zootaxa 4363 (1): 101. https://doi.org/10.11646/zootaxa.4363.1.4

Kaczmarek Ł., Zawierucha K., Buda J., Stec D., Gawlak M., Michalczyk Ł. & Roszkowska M. 2018. An integrative redescription of the nominal taxon for the Mesobiotus harmsworthi group (Tardigrada: Macrobiotidae) leads to descriptions of two new Mesobiotus species from Arctic. PLoS ONE 13 (10): e0204756. https://doi.org/10.1371/journal.pone.0204756

Kiehl E., Dastych H., D’Haese J. & Greveh H. 2007. The 18S rDNA sequences support polyphyly of the Hypsibiidae (Eutardigrada). Journal of Limnology 66 (Suppl. 1): 21–25. https://doi.org/10.4081/jlimnol.2007.s1.21

Kosztyła P., Stec D., Morek W., Gąsiorek P., Zawierucha K., Michno K., Ufir K., Małek D., Hlebowicz K., Laska A., Dudziak M., Frohme M., Prokop Z.M., Kaczmarek Ł. & Michalczyk Ł. 2016. Experimental taxonomy confirms the environmental stability of morphometric traits in a taxonomically challenging group of microinvertebrates. Zoological Journal of the Linnean Society 178: 765–775. https://doi.org/10.1111/zoj.12409

Kristensen R.M. 1982. New aberrant Eutardigrades from homothermic springs on Disko Island, West Greenland. In: Nelson D.R. (ed.) Proceedings of the Third International Symposium on the Tardigrada, August 3-6, 1980, Johnson City, Tennessee, USA: 203–220. East Tennessee State University Press, Johnson City, Tenn., USA.

Kumar S., Stecher G. & Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33 (7): 1870–1874. https://doi.org/10.1093/molbev/msw054

Lisi O. 2015. Current knowledge on the Sicilian tardigrade fauna. Biodiversity Journal 6 (1): 297–304.

Marcus E. 1929. Tardigrada. Akademische Verlagsgesellschaft m.b.H, Leipzig.

Marcus E. 1930. Beiträge zur Tardigradensystematik. Zoologische Jahrbücher Abteilung für Systematik, Ökologie und Geographie der Tiere 59: 363–386

Marcus E. 1936. Tardigrada. Walter de Gruyter & Co., Berlin / Leipzig.

Marley N.J., Mcinnes S.J. & Sands C.J. 2011. Phylum Tardigrada: a re-evaluation of the Parachela. Zootaxa 2819 (1): 51. https://doi.org/10.11646/zootaxa.2819.1.2

Maucci W. 1987. A contribution to the knowledge of the North American Tardigrada with emphasis on the fauna of Yellowstone National Park (Wyoming). In: Bertolani R. (ed.) Biology of Tardigrades: Proceedings of the 4th International Symposium on the Tardigrada, Modena, September 3–5, 1985: 187–210. Mucchi, Modena.

Maucci W. 1988. Tardigrada from Patagonia (Southern South America) with description of three new species. Revista Chilena de Entomología 16: 5–13.

Maucci W. 1996. Tardigrada of the Arctic tundra with descriptions of two new species. Zoological Journal of the Linnean Society 116 (1–2): 185–204. https://doi.org/10.1111/j.1096-3642.1996.tb02343.x

Michalczyk Ł. & Kaczmarek Ł. 2013. The Tardigrada Register: a comprehensive online data repository for tardigrade taxonomy. Journal of Limnology 72 (1s): e22. https://doi.org/10.4081/jlimnol.2013.s1.e22

Miller M.A., Pfeiffer W. & Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: 2010 Gateway Computing Environments Workshop (GCE): 1–8.

Morek W., Stec D., Gąsiorek P., Schill R.O., Kaczmarek Ł. & Michalczyk Ł. 2016. An experimental test of eutardigrade preparation methods for light microscopy. Zoological Journal of the Linnean Society 178 (4): 785–793. https://doi.org/10.1111/zoj.12457

Murray J. 1907a. Scottish Tardigrada collected by the Lake Survey. Transactions of the Royal Society of Edinburgh 45 (3): 641–668. https://doi.org/10.1017/S0080456800011777

Murray J. 1907b. Arctic Tardigrada, collected by Wm. S. Bruce. Transactions of the Royal Society of Edinburgh 45 (3): 669–681. https://doi.org/10.1017/S0080456800011789

Osawa S., Su Z.-H. & Imura Y. 2004. Molecular Phylogeny and Evolution of Carabid Ground Beetles. Springer Japan, Tokyo.

Pilato G. 1969. Evoluzione e nuova sistemazione degli eutardigrada. Bolletino di Zoologia 36 (3): 327–345. https://doi.org/10.1080/11250006909436925

Pilato G. 1981. Analisi di nuovi caratteri nello studio degli Eutardigradi. Animalia 8 (1/3): 51–57.

Pilato G. 1987. Revision of the genus Diphascon Plate, 1889, with remarks on the subfamily Itaquasconinae (Eutardigrada, Hypsibiidae). In: Bertolani R. (ed.) Biology of Tardigrades: Proceedings of the 4th International Symposium on the Tardigrada, Modena, September 3–5, 1985: 337–357. Mucchi, Modena.

Pilato G. 1992. Mixibius, nuovo genere di Hypsibiidae (Eutardigrada). Animalia 19 (1/3): 121–125.

Pilato G. & Binda M.G. 1990. Tardigradi dell Antartide. I. Ramajendas, nuovo genere di Eutardigrado. Nuova posizione sistematica di Hypsibius renaudi Ramazzotti, 1972 e descrizione di Ramajendas frigidus n. sp. Animalia 17: 61–71.

Pilato G. & Binda M.G. 1997. Acutuncus, a new genus of Hypsibiidae (Eutardigrada). Entomologische Mitteilungen aus dem Zoologischen Museum Hamburg 12 (155): 159–162.

Pilato G. & Binda M.G. 2010. Definition of families, subfamilies, genera and subgenera of the Eutardigrada, and keys to their identification. Zootaxa 2404 (1): 1. https://doi.org/10.11646/zootaxa.2404.1.1

Pilato G., Binda M.G. & Claxton S. 2002. Itaquascon unguiculum and Itaquascon cambewarrense. two new species of eutardigrades from Australia. New Zealand Journal of Zoology 29 (2): 87–93. https://doi.org/10.1080/03014223.2002.9518293

Pilato G., Binda M.G. & Lisi O. 2003. Remarks on some species of tardigrades from South America with the description of Minibiotus sidereus n. sp. Zootaxa 195: 1–8. https://doi.org/10.11646/zootaxa.195.1.1

Pilato G., Kiosya Y., Lisi O., Inshina V. & Biserov V. 2011. Annotated list of Tardigrada records from Ukraine with the description of three new species. Zootaxa 3123 (1): 1–31. https://doi.org/10.11646/zootaxa.3123.1.1

Pilato G., Kiosya Y., Lisi O. & Sabella G. 2012. New records of Eutardigrada from Belarus with the description of three new species. Zootaxa 3179: 39–60. https://doi.org/10.11646/zootaxa.3179.1.2

Pleijel F., Jondelius U., Norlinder E., Nygren A., Oxelman B., Schander C., Sundberg P. & Thollesson M. 2008. Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48 (1): 369–371. https://doi.org/10.1016/j.ympev.2008.03.024

Poprawa I. 2005. The structure and the formation of egg shells in the parthenogenetic species Dactylobiotus dispar Murray, 1907 (Tardigrada: Eutardigrada). Folia Biologica 53 (3): 173–177. https://doi.org/10.3409/173491605775142828

Poprawa I. 2011. Ultrastructural studies of the formation of the egg capsule in the hermaphroditic species, Isohypsibius granulifer granulifer Thulin, 1928 (Eutardigrada: Hypsibiidae). Zoological Science 28 (1): 37–40. https://doi.org/10.2108/zsj.28.37

Poprawa I., Schlechte-Wełnicz W. & Hyra M. 2015. Ovary organization and oogenesis in the tardigrade Macrobiotus polonicus Pilato, Kaczmarek, Michalczyk & Lisi, 2003 (Eutardigrada, Macrobiotidae): ultrastructural and histochemical analysis. Protoplasma 252 (3): 857–865. https://doi.org/10.1007/s00709-014-0725-x

Ramazzotti G. & Maucci W. 1983. Il phylum Tardigrada. Istituto Italiano di Idrobiologia, Verbania Pallanza.

Richters F. 1911. Faune des mousses. Tardigrades. Duc d’Orleans, Campagne arctique de 1907. Imprimerie Scientifique C. Belens, Bruxelles.

Ronquist F. & Huelsenbeck J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (12): 1572–1574. https://doi.org/10.1093/bioinformatics/btg180

Sands C.J., McInnes S.J., Marley N.J., Goodall-Copestake W.P., Convey P. & Linse K. 2008. Phylum Tardigrada: an “individual” approach. Cladistics 24 (6): 861–871. https://doi.org/10.1111/j.1096-0031.2008.00219.x

Schuster R.O., Nelson D.R., Grigarick A.A. & Christenberry D. 1980. Systematic criteria of the Eutardigrada. Transactions of the American Microscopical Society 99 (3): 284. https://doi.org/10.2307/3226004

Scotland R.W., Olmstead R.G. & Bennett J.R. 2003. Phylogeny reconstruction: the role of morphology. Systematic Biology 52 (4): 539–548.

Smirnov A., Nassonova E., Berney C., Fahrni J., Bolivar I. & Pawlowski J. 2005. Molecular phylogeny and classification of the lobose amoebae. Protist 156 (2): 129–142. https://doi.org/10.1016/j.protis.2005.06.002

Smith N.D. & Turner A.H. 2005. Morphology’s role in phylogeny reconstruction: perspectives from paleontology. Systematic Biology 54 (1): 166–173. https://doi.org/10.1080/10635150590906000

Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30 (9): 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: 501–526. https://doi.org/10.11646/zootaxa.4052.5.1

Stec D., Gąsiorek P., Morek W., Kosztyła P., Zawierucha K., Michno K., Kaczmarek Ł., Prokop Z.M. & Michalczyk Ł. 2016a. Estimating optimal sample size for tardigrade morphometry. Zoological Journal of the Linnean Society 178 (4): 776–784. https://doi.org/10.1111/zoj.12404

Stec D., Morek W., Gąsiorek P. , Kaczmarek Ł., & Michalczyk Ł. 2016b. 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. & Michalczyk Ł. 2018. 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

Thulin G. 1911. Beiträge zur Kenntnis der Tardigradenfauna Schwedens. Arkiv för zoologi 7: 1–60. https://doi.org/10.5962/bhl.part.1270

Trygvadóttir B.V. & Kristensen R.M. 2011. Eohypsibiidae (Eutardigrada, Tardigrada) from the Faroe Islands with the description of a new genus containing three new species. Zootaxa 2886: 39–62. https://doi.org/10.11646/zootaxa.2886.1.4

Tumanov D.V. 1997. Hypsibius iskandarovi sp. n., a new species of Tardigrada from fresh waters of North-West Russia (Tardigrada: Hypsibiidae). Zoosystematica Rossica 5 (2): 219–220.

Tumanov D.V. 2018. Hypsibius vaskelae, a new species of Tardigrada (Eutardigrada, Hypsibiidae) from Russia. Zootaxa 4399 (3): 434. https://doi.org/10.11646/zootaxa.4399.3.12

Vecchi M., Cesari M., Bertolani R., Jönsson K.I., Rebecchi L. & Guidetti R. 2016. Integrative systematic studies on tardigrades from Antarctica identify new genera and new species within Macrobiotoidea and Echiniscoidea. Invertebrate Systematics 30 (4): 303. https://doi.org/10.1071/IS15033

Velasco-Castrillón A., McInnes S.J., Schultz M.B., Arróniz-Crespo M., D’Haese C.A., Gibson J.A.E., Adams B.J., Page T.J., Austin A.D., Cooper S.J.B. & Stevens M.I. 2015. Mitochondrial DNA analyses reveal widespread tardigrade diversity in Antarctica. Invertebrate Systematics 29 (6): 578-590. https://doi.org/10.1071/IS14019

Węglarska B. 1982. Ultrastructural study of the formation of egg envelopes in Macrobiotus richtersi (Eutardigrada). In: Nelson D.R. (ed.) Proceedings of the Third International Symposium on the Tardigrada, August 3–6, 1980, Johnson City, Tennessee, USA: 115–127. East Tennessee State University Press, Johnson City, Tenn., USA.

Wiens J.J. 2004. The role of morphological data in phylogeny reconstruction. Systematic Biology 53 (4): 653–661. https://doi.org/10.1080/10635150490472959

Zantke J., Wolff C. & Scholtz G. 2008. Three-dimensional reconstruction of the central nervous system of Macrobiotus hufelandi (Eutardigrada, Parachela): implications for the phylogenetic position of Tardigrada. Zoomorphology 127 (1): 21–36. https://doi.org/10.1007/s00435-007-0045-1

Zawierucha K., 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

Published
2020-07-07
How to Cite
Tumanov, D. V. (2020). Integrative redescription of Hypsibius pallidoides Pilato et al., 2011 (Eutardigrada: Hypsibioidea) with the erection of a new genus and discussion on the phylogeny of Hypsibiidae. European Journal of Taxonomy, (681). https://doi.org/10.5852/ejt.2020.681
Issue
No. 681 (2020)
Section
Zoology

Copyright (c) 2020 Denis V. Tumanov

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Creative Commons Copyright Notices

Authors who publish with this journal agree to the following terms:

  1. Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY 4.0) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
  2. Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
  3. Authors are NOT ALLOWED TO post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to taxonomic issues.