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Cytology and Cytogenetics

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Water Bears: The Biology of Tardigrades

Part of the book series: Zoological Monographs ((ZM,volume 2))

Abstract

Several cytological aspects have been considered in tardigrades. Firstly, the cell constancy which is not a true eutely being several mitoses present even after hatching, even though some organs, such epidermis and nervous ganglia, have the same cell number in juveniles and adults. The total number of these cells is species-specific. Then the ultrastructure of cuticle, epidermis, feeding and digestive apparatus, excretory and osmoregulatory organs, muscles, nerve cells, sensory cells and storage cells has been considered. Instead, the ultrastructure of the germ cells has been considered in the chapter on reproduction. With regard to chromosome number and shape, it has been observed that generally there is little difference among the species (n = 5 or n = 6), but several cases of polyploid populations exist, often very similar to diploid populations from a morphological point of view. In most cases the polyploid populations do not have males and reproduce by apomixis. Studies on the genome size have confirmed the presence of polyploid populations, as well as the presence of nuclei with multiple amounts of DNA within the same specimen. The genome size of the tardigrades is always relatively small and does not seem related to phylogenetic lineages. Studies on tardigrade genomes have placed this phylum at the centre of discussions on the evolution of Metazoa and have considered the role of horizontal gene transfer in animal evolution with contrasting results.

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References

  • Altiero T, Rebecchi L (2003) First evidence of achiasmatic male meiosis in the water bears Richtersius coronifer and Macrobiotus richtersi (Eutardigrada, Macrobiotidae). Hereditas 139:116–120

    Article  Google Scholar 

  • Ammermann D (1962) Parthenogenese bei dem Tardigraden Hypsibius dujardini (Doy). Naturwissenschaften 49:1–2

    Article  Google Scholar 

  • Ammermann D (1967) Die Cytologie der Parthenogenese bei dem Tardigraden Hypsibius dujardini. Chromosoma 23:203–213

    Article  CAS  Google Scholar 

  • Arakawa K (2016) No evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. Proc Natl Acad Sci USA 113(22):E3057

    Article  CAS  Google Scholar 

  • Arakawa K, Yoshida Y, Tomita M (2016) Genome sequencing of a single tardigrade Hypsibius dujardini individual. Sci Data 3:160063. https://doi.org/10.1038/sdata.2016.63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avdonina AM, Biserova NM, Bertolani R, Rebecchi L (2007) Ultrastructure of the digestive system of Ramazzottius tribulosus and Macrobiotus richtersi (Eutardigrada) in relationship with diet. J Limnol 66(Suppl 1):5–11

    Article  Google Scholar 

  • Baccetti B, Rosati F (1971) Electron microscopy on tardigrades. III. The integument. J Ultrastruct Res 34:214–243

    Article  CAS  Google Scholar 

  • Bemm F, Weiß CL, Schultz J, Förster F (2016) Genome of a tardigrade: horizontal gene transfer or bacterial contamination? Proc Natl Acad Sci U S A 113:E3054. https://doi.org/10.1073/pnas.1525116113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bertolani R (1970) Mitosi somatiche e costanza cellulare numerica nei Tardigradi. Atti Accad Naz Lincei Rend Ser 8a 49:739–742

    Google Scholar 

  • Bertolani R (1971) Partenogenesi geografica triploide in un Tardigrado (Macrobiotus richtersi). Atti Accad Naz Lincei Rend Ser 8a 50:487–489

    Google Scholar 

  • Bertolani R (1972) Sex ratio and geographic parthenogenesis in Macrobiotus (Tardigrada). Experientia 28:94

    Article  Google Scholar 

  • Bertolani R (1975) Cytology and systematics in Tardigrada. Mem Ist Ital Idrobiol 32(Suppl):17–35

    Google Scholar 

  • Bertolani R (1981) A new genus and five new species of Italian fresh-water tardigrades. Boll Mus Civ St Nat Verona 8:249–254

    Google Scholar 

  • Bertolani R (1982) Cytology and reproductive mechanisms in tardigrades. In: Nelson DR (ed) Proceedings of third international symposium on the Tardigrada. East Tennessee State Univ Press, Johnson City, Tennessee, pp 93–114

    Google Scholar 

  • Bertolani R, Garagna S, Manicardi GC, Redi CA (1987) Macrobiotus pseudohufelandi Iharos as a model for cytotaxonomic study in populations of eutardigrades. Experientia 43:210–213

    Article  Google Scholar 

  • Bertolani R, Garagna S, Manicardi GC, Rebecchi L, Redi CA (1994) New data on the nuclear DNA content in some species of tardigrades. In: Argano A, Cirotto C, Grassi Milano E, Mastrolia L (eds) Contributions to animal biology. Halocynthia, Palermo, pp 103–109

    Google Scholar 

  • Bonifacio A, Guidetti R, Altiero T, Sergo V, Rebecchi L (2012) Nature, source and function of pigments in tardigrades: in vivo Raman imaging of carotenoids in Echiniscus blumi. PLoS One 7(e50162):1–8

    Google Scholar 

  • Boothby TC, Goldstein B (2016) Reply to Bemm et al. and Arakawa: identifying foreign genes in independent Hypsibius dujardini genome assemblies. Proc Natl Acad Sci USA 113(22):E3058. https://doi.org/10.1073/pnas.1601149113

    Article  CAS  PubMed  Google Scholar 

  • Boothby TC, Tenlen JR, Smith FW, Wang JR, Patanella KA, Nishimura EO, Tintori SC, Li Q, Jones CD, Yandell M, Messina DN, Glasscock J, Goldstein B (2015) Evidence for extensive horizontal gene transfer from the draft genome of a Tardigrade. Proc Natl Acad Sci USA 112(52):15976–15981

    Article  CAS  Google Scholar 

  • Boothby TC, Tapia H, Brozena AH, Piszkiewicz S, Smith AE, Giovannini I, Rebecchi L, Pielak GJ, Koshland D, Goldstein B (2017) Tardigrades use intrinsically disordered proteins to survive desiccation. Mol Cell 65:975–984

    Article  CAS  Google Scholar 

  • Bussers JC, Jeuniaux C (1973) Chitinous cuticle and systematic position of Tardigrada. Biochem Syst 1:77–78

    Article  Google Scholar 

  • Czernekova M, Jönsson KI (2016) Mitosis in storage cells of the eutardigrades Richtersius coronifer. Zool J Linn Soc 178:888–896

    Article  Google Scholar 

  • Dewel RA, Clark WH (1973a) Studies on the tardigrades. II. Fine structure of the pharynx of Milnesium tardigradum Doyère. Tissue Cell 5:147–159

    Article  CAS  Google Scholar 

  • Dewel RA, Clark WH (1973b) Studies on the tardigrades. III. Fine structure of the esophagus of Milnesium tardigradum Doyère. Tissue Cell 5:161–169

    Article  CAS  Google Scholar 

  • Dewel RA, Dewel WC (1979) Studies on the tardigrades. IV. Fine structure of the hindgut of Milnesium tardigradum Doyère. J Morphol 161:79–109

    Article  Google Scholar 

  • Dewel RA, Roush BG, Dewel WC (1989) Fine structure of the midgut cells of the heterotardigrade Echiniscus viridissimus. Am Zool 28:149A

    Google Scholar 

  • Dewel RA, Dewel WC, Roush BG (1992) Unusual cuticle-associated organs in the heterotardigrade, Echiniscus viridissimus. J Morphol 212:123–140

    Article  Google Scholar 

  • Dewel RA, Nelson DR, Dewel WC (1993) Tardigrada. In: Microscopic anatomy of invertebrates, Onychophora, Chilopoda, and lesser Protostomata, vol 12. Wiley, Hoboken, pp 143–183

    Google Scholar 

  • Greven H (1979) Notes on the structure of vasa Malpighii in the eutardigrade Isohypsibius augusti (Murray 1907). Zesz Nauk Uniw Jagiellon Prace Zool 25:87–96

    Google Scholar 

  • Greven H (1984) Tardigrada. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument Invertebrates, vol 1. Springer, Berlin, pp 714–727

    Chapter  Google Scholar 

  • Greven H, Kuhlmann D (1972) Die Struktur des Nervengewebes von Macrobiotus hufelandi C.A.S. Schultze (Tardigrada). Z Zellforsch 132:131–146

    Article  CAS  Google Scholar 

  • Greven H, Peters W (1986) Localization of chitin in the cuticle of Tardigrada using wheat germ agglutinin-gold conjugate as a specific electron-dense marker. Tissue Cell 18:297–304

    Article  Google Scholar 

  • 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). Zool Lett 5:1. https://doi.org/10.1186/s40851-018-0113-z

    Article  Google Scholar 

  • Guidetti R, Rebecchi L, Bertolani R, Jönsson KI, Kristensen RM, 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. Zool J Linnean Soc 178:834–845

    Article  Google Scholar 

  • Halberg KA, Møbjerg N (2012) First evidence of epithelial transport in tardigrades: a comparative investigation of organic anion transport. J Exp Biol 215:497–507

    Article  CAS  Google Scholar 

  • Halberg KA, Persson D, Møbjerg N, Wanninger A, Kristensen RM (2009) Myoanatomy of the marine tardigrade Halobiotus crispae (Eutardigrada: Hypsibiidae). J Morphol 270:996–1013

    Article  Google Scholar 

  • Hashimoto T, Horikawa DD, Saito Y, Kuwahara H, Kozuka-Hata H, Shin-I T, Minakuchi Y, Ohishi K, Motoyama A, Aizu T, Enomoto A, Kondo K, Tanaka S, Hara Y, Koshikawa S, Sagara H, Miura T, Yokobori S, Miyagawa M, Suzuki Y, Kubo T, Oyama M, Kohara Y, Fujiyama A, Arakawa K, Katayama T, Toyoda A, Kunieda T (2016) Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein. Nat Commun 7. https://doi.org/10.1038/ncomms12808

  • Hyra M, Rost-Roszkowska MM, Student S, Włodarczyk A, Deperas M, Janelt K, Poprawa I (2016a) Body cavity cells of Parachela during their active life. Zool J Linnean Soc 178:878–887

    Article  Google Scholar 

  • Hyra M, Poprawa I, Włodarczyk A, Student S, Sonakowska L, Kszuk-Jendrysik M, Rost-Roszkowska MM (2016b) Ultrastructural changes in the midgut epithelium of Hypsibius dujardini (Doyère, 1840) (Tardigrada, Eutardigrada, Hypsibiidae) in relation to oogenesis. Zool J Linnean Soc 178:897–906

    Article  Google Scholar 

  • Jönsson KI, Rebecchi L (2002) Experimentally induced anhydrobiosis in the tardigrade Richtersius coronifer: phenotypic factors affecting survival. J Exp Zool 293:578–584

    Article  Google Scholar 

  • Koutsovoulos G, Kumar S, Laetsch DR, Stevens L, Daub J, Conlon C, Maroon H, Thomas F, Aboobaker AA, Blaxter B (2016) No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini. Proc Natl Acad Sci USA 113:5053–5058

    Article  CAS  Google Scholar 

  • Kristensen RM (1976) On the fine structure of Batillipes noerrevangi Kristensen 1976. 1. Tegument and moulting cycle. Zool Anz 197:129–150

    Google Scholar 

  • Kristensen RM (1978) On the structure of Batillipes noerrevangi Kristensen 1978 2. The muscle-attachments and the true cross-striated muscles. Zool Anz 200:173–184

    Google Scholar 

  • Kristensen RM (1981) Sense organs of two marine arthrotardigrades (Heterotardigrada, Tardigrada). Acta Zool 62:27–41

    Article  Google Scholar 

  • Kristensen RM, Neuhaus B (1999) The ultrastructure of the tardigrade cuticle with special attention to marine species. Zool Anz 238:261–281

    Google Scholar 

  • Marchioro T, Rebecchi L, Cesari M, Hansen JG, Viotti G, Guidetti R (2013) Somatic musculature of Tardigrada: phylogenetic signal and metameric patterns. Zool J Linnean Soc 169:580–603. https://doi.org/10.1111/zoj.12079

    Article  Google Scholar 

  • Marcus E (1929) Tardigrada. In: Bronn HG (ed) Klassen und Ordnungen des Tierreichs, vol V. Akademische Verlagsgesellschaft, Leipzig, pp 1–608

    Google Scholar 

  • Møbjerg N, Dahl C (1996) Studies on the morphology and ultrastructure of the Malpighian tubules of Halobiotus crispae Kristensen, 1982 (Eutardigrada). Zool J Linnean Soc 116:85–99

    Article  Google Scholar 

  • Pelzer B, Dastych H, Greven H (2007) The osmoregulatory/excretory organs of the glacier dwelling eutardigrade Hypsibius klebelsbergi Mihelčič 1959 (Tardigrada). Mitt Hamb Zool Mus Inst 104:61–72

    Google Scholar 

  • Persson DK, Halberg KA, Jørgensen A, Møbjerg N, Kristensen RM (2012) Neuroanatomy of Halobiotus crispae (Eutardigrada: Hypsibiidae): tardigrade brain structure supports the clade Panarthropoda. J Morphol 273:1227–1245

    Article  Google Scholar 

  • Persson DK, Halberg KA, Jørgensen A, Møbjerg N, Kristensen RM (2014) Brain anatomy of the marine tardigrade Actinarctus doryphorus (Arthrotardigrada). J Morphol 275:173–190

    Article  Google Scholar 

  • Rebecchi L, Altiero T, Bertolani R (2002) Banding techniques on tardigrade chromosomes: the karyotype of Macrobiotus richtersi (Eutardigrada, Macrobiotidae). Chromosom Res 10:437–443

    Article  CAS  Google Scholar 

  • Rebecchi L, Rossi V, Altiero T, Bertolani R, Menozzi P (2003) Reproductive modes and genetic polymorphism in different populations of the tardigrade Richtersius coronifer (Eutardigrada, Macrobiotidae). Invertebr Biol 122:19–27

    Article  Google Scholar 

  • Redi CA, Garagna S (1987) Cytochemical evaluation of the nuclear DNA content as a tool for taxonomical studies in eutardigrades. In: Bertolani R (ed) Biology of tardigrades, vol 1. Mucchi, Modena, pp 73–80

    Google Scholar 

  • Rost-Roszkowska MM, Poprawa I, Wójtowicz M, Kaczmarek Ł (2011) Ultrastructural changes of the midgut epithelium in Isohypsibius granulifer granulifer Thulin, 1928 (Tardigrada: Eutardigrada) during oogenesis. Protoplasma 248:405–414

    Article  Google Scholar 

  • Shaw K (1974) The fine structure of muscle cells and their attachments in the tardigrade Macrobiotus hufelandi. Tissue Cell 6:431–445

    Article  CAS  Google Scholar 

  • Walz B (1973) Zur Feinstruktur der Muskelzellen des Pharynx-Bulbs von Tardigraden. Z Zellforsch 140:389–399

    Article  CAS  Google Scholar 

  • Walz B (1974) The fine structure of somatic muscles of Tardigrada. Cell Tissue Res 149:81–89

    Article  CAS  Google Scholar 

  • Walz B (1975) Ultrastructure of muscle cells in Macrobiotus hufelandi. Mem Ist Ital Idrobiol 32:425–444

    Google Scholar 

  • Walz B (1978) Electron microscopic investigation of cephalic sense organs of the tardigrade Macrobiotus hufelandi C.A.S. Schultze. Zoomorphologie 89:1–19

    Article  Google Scholar 

  • Walz B (1979) Cephalic sense organs of Tardigrada. Current results and problems. Zesz Nauk Uniw Jagiellon Prace Zool 25:161–168

    Google Scholar 

  • Węglarska B (1975) Studies on the morphology of Macrobiotus richtersi Murray, 1911. Mem Ist Ital Idrobiol 32:445–464

    Google Scholar 

  • Węglarska B (1987a) Studies on the excretory system of Isohypsibius granulifer Thulin (Eutardigrada). In: Bertolani R (ed) Biology of tardigrades, vol 1. Mucchi, Modena, pp 15–24

    Google Scholar 

  • Węglarska B (1987b) Morphology and ultrastructure of the excretory system in Dactylobiotus dispar (Murray) (Eutardigrada). In: Bertolani R (ed) Biology of tardigrades, vol 1. Mucchi, Modena, pp 25–33

    Google Scholar 

  • Węglarska B (1987c) Yolk formation in Isohypsibius (Eutardigrada). Zoomorphology 107:287–292

    Article  Google Scholar 

  • Wiederhoft H, Greven H (1996) Notes on head sensory organs of Milnesium tardigradum Doyère, 1840 (Apochela, Eutardigrada). Zool Anz 238:338–346

    Google Scholar 

  • Yoshida Y, Koutsovoulos G, Laetsch DR, Stevens L, Kumar S, Horikawa DD, Ishino K, Komine S, Kunieda T, Tomita M, Blaxter M, Arakawa K (2017) Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus. bioRxiv 15:e2002266. https://doi.org/10.1101/112664

    Article  Google Scholar 

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Bertolani, R., Rebecchi, L. (2018). Cytology and Cytogenetics. 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_6

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