Abstract
Tardigrade phylogeny is currently the object of intense investigations driven by an increasing amount of molecular data from a broad taxonomic range of tardigrades. New information obtained from these investigations plays a crucial role in establishing a reliable systematic framework of Tardigrada. Importantly, contemporary phylogenetic investigations readily incorporate and reinvestigate morphological characters and character systems. Most of these newer investigations are, however, primarily based on a few conservative nuclear genes (in addition to the mitochondrial COI). Emerging transcriptomic and genomic data sets provide promising new information for future phylogenetic studies.
Currently the traditional major taxa of Tardigrada are still accepted, with Eutardigrada constituted by Apochela and Parachela and Heterotardigrada by Echiniscoidea and Arthrotardigrada. However, the arthrotardigrades seem to be a paraphyletic assemblage of distantly related taxa. During the last decade, major rearrangements have occurred in the parachelan taxa Eohypsibioidea, Hypsibioidea, Isohypsibioidea and Macrobiotoidea. Likewise, progress has been made within Arthrotardigrada and Echiniscoidea, but stable phylogenies have yet to be reached within these major taxa.
At the species level, an integrative approach to taxonomy has recently been implemented. Thus, molecular methods in support of morphological investigations are used to facilitate the identification and characterization of different tardigrade species. Phylogenetic inference methods have been combined with DNA barcoding approaches, and the ITS2 secondary structure has been applied as a marker for taxonomy.
In this review we present the current knowledge of tardigrade phylogeny. We emphasise that major changes likely will occur within the phylogenies of arthrotardigrades and echiniscoideans as additional species and genes are sampled for use in molecular phylogenies. We also foresee that integrative approaches to species identification and description will become more widespread securing a firm basis for future investigations in tardigrade taxonomy and systematics.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Aguinaldo AA, Turbeville JM, Linford LS et al (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493
Bello G, de Zio Grimaldi S (1998) Phylogeny of the genera of the Stygarctidae and related families (Tardigrada: Heterotardigrada). Zool Anz 237:171–183
Bertolani R, Grimaldi D (2000) A new eutardigrade (Tardigrada: Milnesiidae) in amber from Upper Cretaceous (Turonian) of New Jersey. In: Grimaldi D (ed) Studies on fossils in amber, with particular reference to the cretaceous of New Jersey. Backhuys Publishers, Leiden, pp 103–110
Bertolani R, Rebecchi L, Cesari M (2010) A model study for tardigrade identification. In: Nimis PL, Vignes Lebbe R (eds) Tools for identifying biodiversity: progress and problems. EUT-Edizioni Università di Trieste, Trieste, pp 333–339
Bertolani R, Rebecchi L, Giovannini I et al (2011a) DNA barcoding an integrative taxonomy of Macrobiotus hufelandi C.A.S. Schultze 1834, the first tardigrade species to be described, and some related species. Zootaxa 2997:19–36
Bertolani R, Biserov VI, Rebecchi L et al (2011b) Taxonomy and biogeography of tardigrades using an integrated approach: new results on species of the Macrobiotus hufelandi group. Inv Zool 8:23–36
Bertolani R, Guidetti R, Marchioro T et al (2014) Phylogeny of Eutardigrada: new molecular data and their morphological support lead to the identification of new evolutionary lineages. Mol Phylogenet Evol 76:110–126
Binda BG (1978) Risistemazione di alcuni Tardigrada con l’istituzione di un nuova genere di Oreellidae e della nuova famiglia Archechiniscidae. Animalia 5:307–314
Binda MG, Kristensen RM (1986) Notes on the genus Oreella (Oreellidae) and the systematic position of Carphania fluviatilis Binda, 1978 (Carphanidae fam. nov., Heterotardigrada). Animalia 13:9–20
Blaxter M, Elsworth B, Daub J (2004) DNA taxonomy of a neglected animal phylum: an unexpected diversity of tardigrades. Proc R Soc Lond B 271:S189–S192
Blaxter M, Mann J, Chapman T et al (2005) Defining operational taxonomic units using DNA barcode data. Phil Trans R Soc Lond B Biol Sci 360(1462):1935–1943
Borner J, Rehm P, Schill RO et al (2014) A transcription approach to ecdysoan phylogeny. Mol Phylogenet Evol 80:79–87
Brusca RC, Brusca GJ (2003) Invertebrates, 2nd edn. Sinauer Associates, Sunderland, MA, p 895
Budd GE (2001) Tardigrades as ‘stem-group arthropods’: the evidence from the Cambrian fauna. Zool Anz 240:265–279
Campbell LI, Rota-Stabelli O, Edgecombe GD et al (2011) MicroRNAs and phylogenomics resolve the relationships of Tardigrada and suggest that velvet worms are the sister group of Arthropoda. PNAS 108:15920–15924
Cesari M, Bertolani R, Rebecchi L et al (2009) DNA barcoding in Tardigrada: the first case study on Macrobiotus macrocalix Bertolani & Rebecchi 1993 (Eutardigrada, Macrobiotidae). Mol Ecol Res 9:699–706
Cesari M, Giovannini I, Bertolani R et al (2011) An example of problems associated with DNA barcoding in tardigrades: a novel method for obtaining voucher specimens. Zootaxa 3104:42–51
Cesari M, Guidetti R, Rebecchi L et al (2013) A DNA barcoding approach in the study of tardigrades. J Limnol 72:182–198
Coleman AW (2000) The significance of a coincidence between evolutionary landmarks found in mating affinity and a DNA sequence. Protist 151:1–9
Coleman AW (2009) Is there a molecular key to the level of biological species in eukaryotes? A DNA guide. Mol Phylogenet Evol 50:197–203
Coleman AW, Vacquier VD (2002) Exploring the phylogenetic utility of ITS sequences for animals: a test case for abalone (Haliotis). J Mol Evol 54:246–257
Cooper KW (1964) The first fossil tardigrade: Beorn leggi, from Cretaceous Amber. Psyche (Camb) 71(2):41–48
Cuvier GB (1812) Sur un nouveau rapprochement à établir entre les classes qui composant le Règne Animal. Ann Mus Hist 19:73–84
Dabert M, Dastych H, Hohberg K et al (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. Mol Phylogenet Evol 70:70–75
Degma P, Bertolani R, Guidetti R (2009–2016) Actual checklist of Tardigrada species. Ver. 31: 15-12-2016. http://www.tardigrada.modena.unimo.it/miscellanea/Actual%20checklist%20of%20Tardigrada.pdf. Accessed 20 Dec 2016
Dunn CW, Hejnol A, Matus DQ et al (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:665–780
Edgecombe GD (2010) Arthropod phylogeny: an overview from the perspectives of morphology, molecular data and the fossil record. Arthropod Struct Dev 39:74–87
Faurby S, Jørgensen A, Kristensen RM et al (2011) Phylogeography of North Atlantic tidal tardigrades: refugia, cryptic speciation and the history of the Mid Atlantic islands. J Biogeogr 38:1613–1624
Faurby S, Jørgensen A, Kristensen RM et al (2012) Distribution and speciation in marine tidal tardigrades: a test of the roles of climate and geographic isolation. J Biogeogr 39(9):1596–1607
Fujimoto S, Jørgensen A, Hansen JG (2016) A molecular approach to arthrotardigrade phylogeny (Heterotardigrada, Tardigrada). Zool Scr 46(4):496–505
Garey JR, Krotec M, Nelson DR et al (1996) Molecular analysis supports a tardigrade arthropod association. Invert Biol 115:79–88
Giribet G, Carranza S, Baguna J et al (1996) First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Mol Biol Evol 13(1):76–84
Grimaldi de Zio S, d’Addabbo Gallo M (1987) Archechiniscus minutus n. sp. and its systematic position within Arthrotardigrada (Tardigrada: Heterotardigrada). In: Bertolani R (ed) Biology of Tardigrades. Selected symposia and monographs U.Z.I. 1. Mucchi, Modena, pp 253–260
Grothman GT, Johansson C, Chilton G et al (2017) Gilbert Rahm and the status of Mesotardigrada Rahm, 1937. Zool Sci 34(1):5–10
Guidetti R, Bertolani R (2001) Phylogenetic relationships in the Macrobiotidae (Tardigrada: Eutardigrada: Parachela). Zool Anz 240:371–376
Guidetti R, Gandolfi A, Rossi V et al (2005) Phylogenetic analysis in Macrobiotidae (Eutardigrada, Parachela): a combined morphological and molecular approach. Zool Scr 34:235–244
Guidetti R, Rebecchi L, Bertolani R et al (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. Zool J Linn Soc 178(4):834–845
Guil N, Giribet G (2012) A comprehensive molecular phylogeny of tardigrades–adding genes and taxa to a poorly resolved phylum-level phylogeny. Cladistics 28:21–49
Guil N, Jørgensen A, Giribet G et al (2013) Congruence between molecular phylogeny and cuticular design in Echiniscoidea (Tardigrada, Heterotardigrada). Zool J Linn Soc 169(4):713–736
Guil N, Jørgensen A, Kristensen R (2019) An upgraded comprehensive multilocus phylogeny of the Tardigrada tree of life. Zool Scripta 48(1):120–137
Hansen JG, Kristensen RM, Jørgensen A (2012) The armoured marine tardigrades (Arthrotardigrada, Tardigrada). Scientia Danica, series B Biologica 2, The Royal Danish Academy of Sciences and Letters, p 91
Hebert PDN, Cywinska A, Ball SL et al (2003) Biological identifications through DNA barcodes. Proc R Soc Lond (Biol) 270:313–321
Hejnol A, Schnabel R (2005) The eutardigrade Thulinia stephaniae has an indeterminate development and the potential to regulate early blastomere ablations. Development 132:1349–1361
Hejnol A, Obst M, Stamatakis A et al (2009) Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc R Soc Lond (Biol) 276:4261–4270
Jørgensen A (2000) Cladistic analysis of the Echiniscidae Thulin, 1928 (Tardigrada: Heterotardigrada: Echiniscoidea). Steenstrupia 25:11–23
Jørgensen A, Kristensen RM (2004) Molecular phylogeny of Tardigrada – investigation of the monophyly of Heterotardigrada. Mol Phylogenet Evol 32:666–670
Jørgensen A, Faurby S, Hansen JG et al (2010) Molecular phylogeny of Arthrotardigrada (Tardigrada). Mol Phylogenet Evol 54:1006–1015
Jørgensen A, Møbjerg N, Kristensen RM (2011) Phylogeny and evolution of the Echiniscidae (Echiniscoidea, Tardigrada) – an investigation of the congruence between molecules and morphology. J Zool Syst Evol Res 49(Suppl 1):6–16
Kiehl E, Dastych H, D’Haese H et al (2007) The 18S rDNA sequences support polyphyly of the Hypsibiidae (Eutardigrada). J Limnol 66(Suppl 1):21–25
Kinchin IM (1994) Origins and systematics. In: Kinchin IM (ed) The biology of Tardigrades. Portland Press, London, pp 7–13
Kristensen RM (1981) Sense organs of two marine arthrotardigrades (Heterotardigrada, Tardigrada). Acta Zool 62:27–41
Kristensen RM (1987) Generic revision of the Echiniscidae (Heterotardigrada), with a discussion of the origin of the family. In: Bertolani R (ed) Biology of Tardigrades. Selected symposia and monographs U.Z.I. 1. Mucchi, Modena, pp 261–335
Kristensen RM, Higgins RP (1984a) Revision of Styraconyx (Tardigrada: Halechiniscidae), with description of two new species from Disko Bay, West Greenland. Smithson Contr Zool 391:1–40
Kristensen RM, Higgins RP (1984b) A new family of Arthrotardigrada (Heterotardigrada: Tardigrada) from the Atlantic coast of Florida, USA. Trans Am Microsc Soc 103:295–311
Kristensen RM, Renaud-Mornant J (1983) Existence d’Arthrotardigrades semi-benthiques de genres nouveaux de la sous-famille des Styraconyxinae subfam. nov. Cah Biol Mar 24:337–353
Lartillot N, Philippe H (2008) Improvement of molecular phylogenetic inference and the phylogeny of Bilateria. Phil Trans R Soc B 363:1463–1472
Liu J, Dunlop JA (2014) Cambrian lobopodians: a review of recent progress in our understanding of their morphology and evolution. Palaeogeogr Palaeocl 398:4–15
Liu J, Steiner M, Dunlop JA et al (2011) An armoured Cambrian lobopodian from China with arthropod-like appendages. Nature 470:526–530
Maas A, Waloszek D (2001) Cambrian derivatives of the early arthropod stem lineage, pentastomids, tardigrades and lobopodians – an “Orsten” perspective. Zool Anz 240(3/4):451–459
Maas A, Mayer G, Kristensen RM et al (2007) A Cambrian micro-lobodian and the evolution of arthropod locomotion and reproduction. Chin Sci Bull 52(24):3385–3392
Marcus E (1929) Tardigrada. In: Bronn HG (ed) Klassen und Ordnungen des Tier-reichs vol 5 sec 4 part 3, pp 1–609
Marley NJ, McInnes SJ, Sands CJ (2011) Phylum Tardigrada: a re-evaluation of the Parachela. Zootaxa 2819:51–64
Møbjerg N, Andersen K, Hygum L et al (2014) Extreme stress tolerance of the intertidal tardigrade Echiniscoides sigismundi. In: The physiologist, APS intersociety meeting: comparative approaches to grand challenges in physiology, San Diego, California, 5–8 October 2014. Program number 39.3
Møbjerg N, Kristensen RM, Jørgensen A (2016) Data from new taxa infer Isoechiniscoides gen. nov. and increase the phylogenetic and evolutionary understanding of echiniscoidid tardigrades (Echiniscoidea: Tardigrada). Zool J Linn Soc 178:804–818
Moon SY, Kim W (1996) Phylogenetic position of the Tardigrada based on the 18S ribosomal RNA gene sequences. In: McInnes SJ, Norman DB (eds) Tardigrade biology. Zool J Linn Soc 116(1/2):61–69
Müller T, Philippi N, Dandekar T et al (2007) Distinguishing species. RNA 13:1469–1472
Nichols PB, Nelson DR, Garey JR (2006) A family level analysis of tardigrade phylogeny. Hydrobiologia 558:53–60
Nielsen C (1995) Animal evolution: interrelationships of the living phyla. Oxford University Press, Oxford, p 467
Nielsen C (2012) Animal evolution: interrelationships of the living phyla, 3rd edn. Oxford University Press, Oxford, p 402
Padial JM, Miralles A, De la Riva I et al (2010) The integrative future of taxonomy. Front Zool 7:16
Persson D, Halberg KA, Jørgensen A et al (2012) Neuroanatomy of Halobiotus crispae (Eutardigrada: Hypsibiidae): Tardigrade brain structure supports the clade Panarthropoda. J Morph 273:1227–1245
Persson DK, Halberg KA, Jørgensen A et al (2014) Brain anatomy of the marine tardigrade Actinarctus doryphorus (Arthrotardigrada). J Morph 275(2):173–190
Pollock LW (1995) New marine tardigrades from Hawaiian beach sand and phylogeny of the family Halechiniscidae. Invertebr Biol 114:220–235
Rahm G (1937) Eine neue Tardigraden-Ordnung aus den heißen Quellen von Unzen, Insel Kyushu, Japan. Zool Anz 120:65–71
Ramazzotti G, Maucci W (1983) Il Phylum Tardigrada. Terza edizione riveduta e corretta. Memorie dell’Isituto Italiano di Idrobiologia Dott. Marco De Marchi 1–1012:41 (English translation by Clark W. Beasley)
Regier JC, Shultz JW, Kambic RE et al (2004) Robust support for tardigrade clades and their ages from three protein-coding nuclear genes. Invertebr Biol 123:93–100
Renaud-Mornant J (1982) Species diversity in marine Tardigrada. In: Nelson D (ed) Proceedings of the Third International Symposium on Tardigrada, Johnson City, Tennessee, 1980. East Tennessee State University Press, Tennessee, pp 149–178
Renaud-Mornant J (1984) Halechiniscidae (Heterotardigrada) de la campagne Benthedi, canal du Mozambique. Bull Mus natn Hist nat Paris 6(1):67–88
Renaud-Mornant J (1987) Halechiniscidae nouveaux de sables coralliens tropicaux (Tardigrada, Arthrotardigrada). Bull Mus natn Hist nat Paris 9(2):353–373
Richters F (1926) Tardigrada. In: Kükenthal W, Krumbach T (eds) Handbuch der Zoologie III. Walter de Gruyter, Berlin, pp 58–61
Rota-Stabelli O, Kayal E, Gleeson D et al (2010) Ecdysozoan mitogenomics: evidence for a common origin of the legged invertebrates, the Panarthropoda. Genome Biol Evol 2:425–440
Rota-Stabelli O, Daley AC, Pisani D (2013) Molecular timetrees reveal a Cambrian colonization of land and a new scenario for ecdysozoan evolution. Curr Biol 23:392–398
Ruppert EE, Fox RS, Barnes RD (2003) Invertebrate zoology: a functional evolutionary approach, 7th edn. Cengage Learning, Hampshire, p 1008
Sands CJ, McInnes SJ, Marley NJ et al (2008) Phylum Tardigrada: an “individual” approach. Cladistics 24:1–11
Schill RO, Förster F, Dandekar T et al (2010) Using compensatory base change analysis of internal transcribed spacer 2 secondary structures to identify three new species in Paramacrobiotus (Tardigrada). Org Divers Evol 10:286–296
Schmidt-Rhaesa A (2001) Tardigrades – are they really miniaturized dwarfs? Zool Anz 240:549–555
Schulte R, Miller WR (2011) Tardigrades of North America: the elevation of a new genus from California. In: Abstracts of the 143rd annual meeting of the Kansas Academy of Science, Baker University, Baldwin City, Kansas, 8–9 April 2011. Transactions of the Kansas Academy of Science 114(1/2):177
Schultz J, Wolf M (2009) ITS2 sequence-structure analysis in phylogenetics. A how to manual for molecular systematics. Mol Phylogenet Evol 52:520–523
Schulz E (1953) Eine neue Tardigradengattung von der pazifischen Küste. Zool Anz 151:306–310
Telford MJ, Bourlat SJ, Economou A et al (2008) The evolution of the Ecdysozoa. Phil Trans R Soc Lond B Biol Sci 363:1529–1537
van Nues RW, Rientjes MJ, Morré SA et al (1995) Evolutionarily conserved structural elements are critical for processing of Internal Transcribed Spacer 2 from Saccharomyces cerevisiae precursor ribosomal RNA. J Mol Biol 250:24–36
Vecchi M, Cesari M, Bertolani R et al (2016) Integrative systematic studies on tardigrades from Antarctica identify new genera and new species within Macrobiotoidea and Echiniscoidea. Invertebr Syst 30:303–322
Vicente F, Fontoura P, Cesari M et al (2013) Integrative taxonomy allows the identification of synonymous species and the erection of a new genus of Echiniscidae (Tardigrada, Heterotardigrada). Zootaxa 3613(6):557–572
Walossek D, Müller KJ, Kristensen RM (1994) A more than half a billion years old stem-group tardigrade from Sibiria. In: Sixth International Symposium on Tardigrada, Selwyn College, Cambridge, 22–26 August 1994
Wełnicz W, Grohme MA, Kaczmarek Ł et al (2011) ITS-2 and 18S rRNA data from Macrobiotus polonicus and Milnesium tardigradum (Eutardigrada, Tardigrada). J Zool Syst Evol Res 49(1):34–39
Acknowledgements
We are grateful to scientific illustrator Stine Elle for her drawings of animals in the cladograms. Funding came from the Carlsberg Foundation and the Danish Council for Independent Research (grant no. DFF – 4090-00145).
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Jørgensen, A., Kristensen, R.M., Møbjerg, N. (2018). Phylogeny and Integrative Taxonomy of Tardigrada. In: Schill, R. (eds) Water Bears: The Biology of Tardigrades. Zoological Monographs, vol 2. Springer, Cham. https://doi.org/10.1007/978-3-319-95702-9_3
Download citation
DOI: https://doi.org/10.1007/978-3-319-95702-9_3
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-95701-2
Online ISBN: 978-3-319-95702-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)