Abstract
Even though tardigrades have been known since 1772, their phylogenetic position is still controversial. Tardigrades are regarded as either the sister group of arthropods, onychophorans, or onychophorans plus arthropods. Furthermore, the knowledge about their gametogenesis, especially oogenesis, is still poor and needs further analysis. The process of oogenesis has been studied solely for several eutardigradan species. Moreover, the spatial organization of the female germ-line clusters has been described for three species only. Meroistic ovaries characterize all analyzed species. In species of the Parachela, one cell per germ-cell cluster differentiates into the oocyte, while the remaining cells become the trophocytes. In Apochela several cells in the cluster differentiate into oocytes. Vitellogenesis is of a mixed type. The eggs are covered with the egg capsule that is composed of two shells: the thin vitelline envelope that adheres to the oolemma and the thick three-layered chorion. Chorion is formed as a first followed by vitelline envelope. Several features related to the oogenesis and structure of the ovary confirm the hypothesis that tardigrades are the sister group rather for arthropods than for onychophorans.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Altiero T, Rebecchi L (2001) Rearing tardigrades: results and problems. Zool Anz 240(3-4):217–221
Amini R, Goupil E, Labella S, Zetka M, Maddox AS, Labbé J-C, Chartier NT (2014) C. elegans Anillin proteins regulate intercellular bridge stability and germline syncytial organization. J Cell Biol 206:129–143
Anderson E, Huebner E (1968) Development of the oocyte and its accessory cells of the polychaete Diopatra cuprea (Bosc). J Morphol 126:163–197
Bertolani R (1972) La partenogenesi nei Tardigradi. Boll Zool 39:577–581
Bertolani R (1979) Hermaphoditism in Tardigrades. Int J Invertebr Reprod 1:67–71
Bertolani R (1983) Tardigrada. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, Oogenesis, oviposition and oosorption, vol I. Wiley, Chichester, pp 431–441
Bertolani R (1987) Sexuality, reproduction and propagation in tardigrades. In: Bertolani R (ed.), Biology of tardigrades. Proceedings of fourth international symposium Tardigrada, Modena. Selected Symposia and Monographs, U.Z.I. 1 Mucchi, Modena, pp 93–101
Bertolani R (2001) Evolution of the reproductive mechanisms in tardigrades – a review. Zool Anz 240(3):247–252
Bertolani R, Manicardi GC (1986) New cases of hermaphroditism in tardigrades. Int J Invert Reprod Dev 9(3):363–366
Bertolani R, Pilato G, Sabatini MA (1983) Macrobiotus joannae, primo macrobiotidae ermafrodito (Eutardigrada). Animal 10:327–333
Bertolani R, Rebecchi L, Claxton SK (1996) Phylogenetic significance of egg shell variation in tardigrades. Zool J Linnean Soc 116:139–148
Biliński SM (1979) Powstawanie żółtka w oogenezie bezkręgowców. Post Biol Kom 6(4):249–266
Bilinski SM (1994) The ovary of Entognatha. In: Büning J (ed) The insect ovary: ultrastructure, previtellogenic growth and evolution. Chapman and Hall, London, pp 7–30
Bilinski SM (1998) Introductory remarks. Folia Histochem Cytobiol 36:143–145
Binda MG, Kristiensen RM (1986) Notes on the genus Oreella (Oreellidae) and the systematic position of Carphania fluviatilis Binda, 1978 (Carphanidae fam. nov., Heterotardigrada). Animal 13:9–20
Brubacher JL, Huebner E (2009) Development of polarized female germline cysts in the polychaete, Ophryotrocha labronica. J Morphol 270:413–429
Brubacher JL, Huebner E (2011) Evolution and development of polarized germ cell cysts: new insights from a polychaete worm Ophryotrocha labronica. Dev Biol 357:96–107
Büning J (1994) The Insect Ovary: Ultrastructure, previtellogenic growth and evolution. Chapman and Hall, London
Crowe JH (1975) The physiology of cryptobiosis in tardigrades. Mem Ist Ital Idrobiol 32:37–59
Czerneková M, Jönsson KI, Chajec L, Student S, Poprawa I (2017) The structure of the desiccated Richtersius coronifer (Richters, 1903). Protoplasma 254(3):1367–1137
Czerneková M, Jönsson KI, Chajec L, Student S, Poprawa I (2018) A comparative ultrastructure study of storage cells in the eutardigrade Richtersius coronifer in the hydrated state and after desiccation and heating stress. PLoS One 13(8):e0201430. https://doi.org/10.1371/journal.pone.0201430
Degma P, Bertolani R, Guidetti R (2009–2018) Actual checklist of Tardigrada species (2009 2018, Ver. 34: Edition: 30-06-2018)
Dewel RA, Nelson DR, Dewel WC (1993) Tardigrada. In: Harrison FW, Rice ME (eds) Microscopic Anatomy of Invertebrates. Onychophora, Chilopoda and Lesser Protostomata, vol 12. Wiley-Liss, New York, pp 143–183
Eckelbarger KJ (1994) Diversity of metazoan ovaries and vitellogenic mechanisms – implications for life history theory. Proc Biol Soc Wash 107:193–218
Foor WE (1968) Cytoplasmic bridges in the ovary of Ascaris lumbricoides. Bull Tulane Univ Med Fac 27:23–30
Foor WE (1983) Nematoda. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, vol I. Oogenesis, oviposition, and oosorption. Wiley, Chichester, pp 223–256
Gibert MA, Starck J, Beguet B (1984) Role of the gonad cytoplasmic core during oogenesis of the nematode Caenorhabditis elegans. Biol Cell 50:77–85
Greenbaum MP, Iwamori T, Buchold GM, Matzuk MM (2011) Germ cell intercellular bridges. Cold Spring Harb Perspect Biol 3:a005850
Grimaldi de Zio S, D’Addabbo Gallo M, Morone de Lucia MR, D’Addabbo L (1987) Marine Arthrotardigrade and Echiniscoidea (Tardigrada, Heterotardigrada) from the Indian Ocean. Boll Zool (4):347–357
Grothman GT, Carl Johansson C, Chilton G, Kagoshima H, Tsujimoto M, Suzuki AC (2017) Gilbert Rahm and the Status of Mesotardigrada Rahm, 1937. Zool Sci 34(1):5–10
Haglund K, Nezis IP, Stenmark H (2011) Structure and functions of stable intercellular bridges formed by incomplete cytokinesis during development. Commun Integr Biol 4:1–9
Horikawa DD (2012) Survival of tardigrades in extreme environments: a model animal for astrobiology. In: Altenbach AV, Bernhard JM, Seckbach J (eds) Anoxia. Evidence for eukaryote survival and paleontological strategies. Springer, Dordrecht, pp 205–217
Huynh JRR, St Johnston D (2004) The origin of asymmetry: early polarisation of the Drosophila germline cyst and oocyte. Curr Biol 14:438–449
Hyra M, Rost-Roszkowska MM, Student S, Włodarczyk A, Deperas M, Janelt K, Poprawa I (2016) Body cavity cells of Parachela during their active life. Zool J Linnean Soc 178:878–887
Jaglarz MK, Kubrakiewicz J, Jedrzejowska I, Goldyn B, Bilinski SM (2014a) Ultrastructural analysis of the ovary and oogenesis in Spinicaudata and Laevicaudata (Branchiopoda) and its phylogenetic implications. Zoology 117:207–215
Jaglarz MK, Kubrakiewicz J, Bilinski SM (2014b) The ovary structure and oogenesis in the basal crustaceans and hexapods. Possible phylogenetic significance. Arthropod Struct Dev 43:349–360
Jędrzejowska I, Mazurkiewicz-Kania M, Garbiec A, Kubrakiewicz J (2013) Differentiation and function of the ovarian somatic cells in the pseudoscorpion, Chelifer cancroides (Linnaeus, 1761) (Chelicerata: Arachnida: Pseudoscorpionida). Arthropod Struct Dev 42:27–36
Keilin D (1959) The Leeuwenhoek lecture. The problem of anabiosis or latent life: history and current concept. Proc R Soc London B 150:149–191
Kinchin IM (1994) The biology of tardigrades. Portland, London
Kloc M, Bilinski S, Dougherty MT, Brey EM, Etkin LD (2004) Formation, architecture and polarity of female germline cyst in Xenopus. Dev Biol 266(1):43–61
Kristensen RM (1977) On the marine genus Styraconyx (Tardigrada, Heterotardigrada, Halechiniscidae) with description of a new species from a warm spring on Disco Island, West Greenland. Astarte 10:87–91
Kubrakiewicz J (1997) Germ cells cluster organization in polytrophic ovaries of Neuroptera. Tissue Cell 29:221–228
Kubrakiewicz J (1998) Struktura i funkcja zespołów komórek płciowych w politroficznych owariolach sieciarek (Insecta: Neuroptera). Rozprawa habilitacyjna. Wydawnictwo Uniwersytetu Wrocławskiego, Wrocław
Kubrakiewicz J, Adamski RT, Biliński SM (1991) Ultrastructural studies on accessory nuclei in developing oocytes of the crustacean, Siphonophanes grubei. Tissue Cell 23:903–907
Lin H, Spradling AC (1995) Fusome asymmetry and oocyte determination in Drosophila. Dev Genet 16:6–12
Marcus E (1929) Tardigrada. In: Bronn HG (ed) Klassen und Ordungen des Tierreichs, vol 5, Section 4, Part 3, pp 1-608
Margaritis LH (1985) Structure and physiology of the eggshell. In: Gilbert LI, Kerkut GA (eds) Comprehensive insect biochemistry physiology and pharmacology 1, vol 6. Pergamon, Berlin, pp 151–230
Matova N, Cooley L (2001) Comparative aspects of animal oogenesis. Dev Biol 231:291–320
Mayer G, Tait NN (2009) Position and development of oocytes in velvet worms shed light on the evolution of the ovary in Onychophora and Arthropoda. Zool J Linnean Soc 157:17–33
Mayer G, Martin C, Rüdiger J, Kauschke S, Stevenson PA, Poprawa I, Hohberg K, Schill RO, Pflüger HJ, Schlegel M (2013) Selective neuronal staining in tardigrades and onychophorans provides insights into the evolution of segmental ganglia in panarthropods. BMC Evol Biol 13:230
Nelson DR (1982) Tardigrada. In: Hurlbert SH, Villalobos-Figueroa A (eds) Aquatic biota of Mexico, Central America and the West Indies. San Diego State University Press, San Diego, pp 154–158
Nelson DR (2002) Current status of Tardigrada: evolution and ecology. Integr Comp Biol 42:652–659
Nelson DR, Guidetti R, Rebecchi L (2015) Phylum Tardigrada. In: Thorp J, Rogers DC (eds) Thorp and Covich’s freshwater invertebrates. Ecology and general biology, vol 1, 4th edn. Elsevier, Oxford, pp 347–380
Nielsen C (2001) Animal evolution: Interrelationships of the living phyla, 2nd edn. Oxford University Press, Oxford
Norman JM, Tait NN (2008) Ultrastructure of the eggshell and its formation in Planipapillus mundus (Onychophora: Peripatopsidae). J Morphol 269:1263–1275
Ong S, Tan C (2010) Germline cyst formation and incomplete cytokinesis during Drosophila melanogaster oogenesis. Dev Biol 337:84–98
Pollock LW (1970) Reproductive anatomy of some marine Heterotardigrada. Trans Am Microsc Soc 89:308–316
Pollock LW (1975) Tardigrada. In: Giese AC, Pearse JS (eds) Reproduction of marine invertebrates, vol 2. Academic, New York, pp 43–54
Poprawa I (2005a) The ovary structure, previtellogenic and vitellogenic stages in parthenogenetic species Dactylobiotus dispar (Murray, 1907) (Tardigrada: Eutardigrada). Tissue Cell 37:385–392
Poprawa I (2005b) The structure and the formation of egg shells in parthenogenetic species Dactylobiotus dispar Murray, 1907 (Tardigrada: Eutardigrada). Folia Biol (Krakow) 53:173–177
Poprawa I (2006) Ultrastuctural changes of the storage cells during oogenesis in Dacylobiotus dispar (Murray, 1907) (Tardigrada: Eutardigrada). Zool Pol 51:13–18
Poprawa I (2011) Ultrastructural studies of the formation of the egg capsule in the hermaphroditic species, Isohypsibius granulifer granulifer Thulin, 1928 (Eutardigrada: Hypsibiidae). Zool Sci 28(1):37–40
Poprawa I, Baran A, Rościszewska E (2002) Structure of ovaries and formation of egg envelopes in the stonefly, Leuctra autumnalis Aubert, 1948 (Plecoptera: Leuctridae). Ultrastructural studies. Folia Biol (Cracow) 50:29–38
Poprawa I, Hyra M, Kszuk-Jendrysik M, Rost-Roszkowska MM (2015a) Ultrastructural changes and programmed cell death of trophocytes in the gonad of Isohypsibius granulifer granulifer (Tardigrada, Eutardigrada, Isohypsibiidae). Micron 70:26–33
Poprawa I, Hyra M, Rost-Roszkowska MM (2015b) Germ cell cluster organization and oogenesis in the tardigrade Dactylobiotus parthenogeneticus Bertolani, 1982 (Eutardigrada, Murrayidae). Protoplasma 252:1019–1029
Poprawa I, Schlechte-Wełnicz W, Hyra M (2015c) Ovary organization and oogenesis in the tardigrade Macrobiotus polonicus Pilato, Kaczmarek, Michalczyk & Lisi, 2003 (Eutardigrada, Macrobiotidae): ultrastructural and histochemical analysis. Protoplasma 252:857–865
Rahm G (1937) Eine neue Tardigraden-ordnung aus den heissen Quellen von Unzen, Insel Kyushu, Japan. Zool Anz 121:65–71
Ramazzotti G, Maucci W (1983) Il Phylum Tardigrada. III edizione riveduta e aggiomata. Mem Ist Ital Idrobiol 41:1–1012 (an English translation, ed. by Dr. C. Beasley)
Rebecchi L (1997) Ultrastructural study of spermiogenesis and the testicular and spermathecal spermatozoon of the gonochoristic tardigrade Xerobiotus pseudohufelandi (Eutardigrada, Macrobiotidae). J Morphol 234(1):11–24
Rebecchi L, Bertolani R (1994) Maturative pattern of ovary and testis in eutardigrades of freshwater and terrestrial habitats. Invertebr Reprod Dev 26(2):107–117
Rebecchi L, Nelson DR (1998) Evaluation of a secondary sex character in eutardigrades. Invertebr Biol 117(3):194–198
Rebecchi L, Altiero T, Cesari M, Bertolani R, Rizzo AM, Corsetto PA, Guidetti R (2011) Resistance of the anhydrobiotic eutardigrade Paramacrobiotus richtersi to space flight (LIFE-TARSE mission on FOTON-M3). J Zool Syst Evol Res 49(Suppl 1):98–103
Renaud-Debyser J (1965) Parastygarctus higginsi n. g., n. sp., tardigrade marin interstitiel de Madagascar. C R Acad Sci 260:955–957
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
Rota-Stabelli O, Kayal E, Gleeson D, Daub J, Boore JL, Telford MJ, Pisani D, Blaxter M, Lavrov DV (2010) Ecdysozoan mitogenomics: evidence for a common origin of the legged invertebrates, the Panarthropoda. Genome Biol Evol 2:425–440
Suzuki A (2006) Ovarian structure in Milnesium tardigradum (Tardigrada: Milnesiidae) during early vitellogenesis. Hydrobiologia 558:61–66
Świątek P, Kubrakiewicz J, Klag J (2009) Formation of germ-line cysts with a central cytoplasmic core is accompanied by specific orientation of mitotic spindles and partitioning of existing intercellular bridges. Cell Tissue Res 337:137–148
Świątek P, De Wit P, Jarosz N, Chajec Ł, Urbisz AZ (2018) Micromorphology of ovaries and oogenesis in Grania postclitellochaeta (Clitellata: Enchytraeidae). Zoology 126:119–127
Szymańska B (1994) Interdependence between storage bodies and egg developmental stages in Macrobiotus richtersi Murray, 1911 (Tardigrada). Acta Biol Cracov Ser Zool 36:41–50
Telford MJ, Bourlat SJ, Economou A, Papillon D, Rota-Stabelli O (2008) The evolution of the Ecdysozoa. Philos Trans R Soc Lond Ser B Biol Sci 363(1496):1529–1537
Tsujimoto M, Imura S, Kanda H (2015) Recovery and reproduction of an Antarctic tardigrade retrieved from a moss sample frozen for over 30 years. Cryobiology 72(1):78–81
Tworzydło W, Biliński SM (2008) Structure of ovaries and oogenesis in dermapterans. I. Origin and functioning of the ovarian follicles. Arthropod Struct Dev 37:310–320
Tworzydło W, Biliński SM, Kočárek P, Haas F (2010) Ovaries and germline cysts and their evolution in Dermaptera (Insecta). Arthropod Struct Dev 39:360–368
Urbisz AZ, Chajec Ł, Brąszewska-Zalewska A, Kubrakiewicz J, Świątek P (2017) Ovaries of the white worm (Enchytraeus albidus, Annelida, Clitellata) are composed of 16-celled meroistic germ-line cysts. Dev Biol 426:28–42
Urbisz AZ, Chajec Ł, Ito M, Ito K (2018) The ovary organization in the marine limnodriloidin Thalassodrilides cf. briani (Annelida: Clitellata: Naididae) resembles the ovary of freshwater tubificins. Zoology 128:16–26
Volkman A, Greven H (1993) Ultrastructural localization of tyrosinase in the tardigrade cuticle. Tissue Cell 25:435–438
Węglarska B (1975) Studies on the morphology of Macrobiotus richtersi Murray, 1911. Mem Ist Ital Idrobiol 32:445–464
Węglarska B (1979) Electron microscope study of previtellogenesis and vitellogenesis in Macrobiotus richtersi J. Murr. (Eutardigrada). Zesz Nauk Uniw Jagiell Pr Zool 25:169–189
Węglarska B (1982) Ultrastructural study of the formation of egg envelopes in Macrobiotus richtersi (Eutardigrada). In: Nelson DR (ed) Proceedings of third international symposium Tardigrada. East Tennessee State University Press, Johnson City, pp 115–128
Węglarska B (1987) Yolk formation in Isohypsibius (Eutardigrada). Zoomorphology 107:287–292
Wełnicz W, Grohme MA, Kaczmarek Ł, Schill RO, Frohme M (2011) Anhydrobiosis in tardigrades: the last decade. J Insect Physiol 57(5):577–583
Wright JC, Westh P, Ramløv H (1992) Cryptobiosis in Tardigrada. Biol Rev 67:1–29
Acknowledgments
We are grateful to Dr. Łukasz Kaczmarek (Department of Animal Taxonomy and Ecology, Faculty of Biology, Adam Mickiewicz University, Poznań, Poland), MSc Milena Roszkowska (Department of Bioenergetics, Institute of Molecular Biology and Biotechnology, Adam Mickiewicz University, Poznań, Poland), MSc Magdalena Gawlak (Institute of Plant Protection-National Research Institute, Poznań, Poland), and MSc Marta Jezierska (Department of Animal Histology and Embryology, University of Silesia in Katowice, Poland) for agreeing to the use of some of their photographic documentation.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Poprawa, I., Janelt, K. (2019). Reproduction, Gonad Structure, and Oogenesis in Tardigrades. In: Tworzydlo, W., Bilinski, S. (eds) Evo-Devo: Non-model Species in Cell and Developmental Biology. Results and Problems in Cell Differentiation, vol 68. Springer, Cham. https://doi.org/10.1007/978-3-030-23459-1_20
Download citation
DOI: https://doi.org/10.1007/978-3-030-23459-1_20
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-23458-4
Online ISBN: 978-3-030-23459-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)