Advertisement

Cell and Tissue Research

, Volume 377, Issue 3, pp 369–382 | Cite as

The digestive system of xenacoelomorphs

  • B. Gavilán
  • S. G. Sprecher
  • V. HartensteinEmail author
  • P. MartinezEmail author
Review

Abstract

Interest in the study of Xenacoelomorpha has recently been revived due to realization of its key phylogenetic position as the putative sister group of the remaining Bilateria. Phylogenomic studies have attracted the attention of researchers interested in the evolution of animals and the origin of novelties. However, it is clear that a proper understanding of novelties can only be gained in the context of thorough descriptions of the anatomy of the different members of this phylum. A considerable literature, based mainly on conventional histological techniques, describes different aspects of xenacoelomorphs’ tissue architecture. However, the focus has been somewhat uneven; some tissues, such as the neuro-muscular system, are relatively well described in most groups, whereas others, including the digestive system, are only poorly understood. Our lack of knowledge of the xenacoelomorph digestive system is exacerbated by the assumption that, at least in Acoela, which possess a syncytial gut, the digestive system is a derived and specialized tissue with little bearing on what is observed in other bilaterian animals. Here, we try to remedy this lack of attention by revisiting the different studies of the xenacoelomorph digestive system, and we discuss the diversity present in the light of new evolutionary knowledge.

Keywords

Xenacoelomorpha Xenoturbella Nemertodermatida Acoela Digestive system Syncytium Lumen Ultrastructure 

Notes

Acknowledgments

We would like to thank Dr. Olga Raikova (Saint Petersburg, Russia) for helping us clarifying some ultrastructural details of the Acoela that were needed for this review. Prof. Julian P.S. Smith III (Winthrop University, USA) kindly sent us a copy of his, comprehensive, PhD thesis on acoel digestive systems. Dr. Kennet Lundin (Gothenburg Natural History Museum, Sweden) was also instrumental in helping us to understand some aspects of the nemertodermatids’ digestive system.

The Meara stichopi stained section was provided by Dr. John Buckland-Nicks (Antigonish, Nova Scotia, Canada). Sections of Xenoturbella bocki were obtained from Michaela Egertova and Dr. Maurice Elphick (London, UK) and processed in house.

We would like to thank the anonymous referees for helping us to improve the manuscript.

Funding

V: H. would like to acknowledge the financial support provided by the NIH (NIH Grant 1RO1 R01 NS054814 to V.H.). PM and SGS would like to thank the financial support provided by the “KVA fund for internationalization and scientific renewal at the Sven Lovén Centre” that allowed them to collect Xenoturbella specimens in Sweden. In addition, SGS would like to thank the support provided by the COST SNF Grant IZCOZ0_182957.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

References

  1. Achatz JG, Martinez P (2012) The nervous system of Isodiametra pulchra (Acoela) with a discussion on the neuroanatomy of the Xenacoelomorpha and its evolutionary implications. Front Zool 9(1):27.  https://doi.org/10.1186/1742-9994-9-27 CrossRefGoogle Scholar
  2. Achatz JG et al (2013) The Acoela: on their kind and kinships, especially with nemertodermatids and xenoturbellids (Bilateria incertae sedis). Org Divers Evol 13(2):267–286.  https://doi.org/10.1007/s13127-012-0112-4 CrossRefGoogle Scholar
  3. Andrikou C, Thiel D, Ruiz-Santiesteban JA, Hejnol A (n.d.) Excretion through digestive tissues predates the evolution of excretory organs. bioRxiv (136788)Google Scholar
  4. Arboleda E et al (2018) An emerging system to study photosymbiosis, brain regeneration, chronobiology, and behavior: the marine Acoel Symsagittifera roscoffensis. BioEssays 40(10):e1800107.  https://doi.org/10.1002/bies.201800107 CrossRefGoogle Scholar
  5. Arroyo AS et al (2016) Hidden diversity of Acoelomorpha revealed through metabarcoding. Biol Lett 12(9).  https://doi.org/10.1098/rsbl.2016.0674
  6. Baguñà J, Riutort M (2004) The dawn of bilaterian animals: the case of acoelomorph flatworms. BioEssays 26(10):1046–1057.  https://doi.org/10.1002/bies.20113. CrossRefGoogle Scholar
  7. Beltagi S, Mandura AS (1991) Hofstenia arabiensis Nov . Sp . ( Hofsteniidae ): a new species of Acoelan Turbellaria from the Red Sea north of J eddah. JKAU: Sci 3:65–90CrossRefGoogle Scholar
  8. Bery A et al (2010) Structure of the central nervous system of a juvenile acoel, Symsagittifera roscoffensis. Dev Genes Evol 220(3–4):61–76.  https://doi.org/10.1007/s00427-010-0328-2 CrossRefGoogle Scholar
  9. Børve A, Hejnol A (2014) Development and juvenile anatomy of the nemertodermatid Meara stichopi (bock) Westblad 1949 (Acoelomorpha). Front Zool 11:50.  https://doi.org/10.1186/1742-9994-11-50 CrossRefGoogle Scholar
  10. Bourlat SJ et al (2008) Feeding ecology of Xenoturbella bocki (phylum Xenoturbellida) revealed by genetic barcoding. Mol Ecol Resour 8(1):12–22.  https://doi.org/10.1111/j.1471-8286.2007.01959.x CrossRefGoogle Scholar
  11. Buckland-Nicks, J., Lundin, K. Wallberg A (2019) The sperm of Xenacoelomorpha revisited: implications for the evolution of early bilaterians.  https://doi.org/10.1007/s00435-018-0425-8
  12. Corrêa DD (1960) Two new marine Turbellaria from Florida. Bull Mar Sci Gulf Carrib 10:208–216Google Scholar
  13. Crezée M, Tyler S (1976) Hesiolicium gen.N. (Turbellaria Acoela) and observations on its ultrastructure. Zool Scr 5(1–4):207–216.  https://doi.org/10.1111/j.1463-6409.1976.tb00700.x CrossRefGoogle Scholar
  14. Dorey AE (1965) ‘The organization and replacement of the epidermis in acoelous turbellarians.’, Q. J Microsc Sci 106:147–172Google Scholar
  15. Drobysheva IM (1986) Physiological regeneration of the digestive parenchyma in Convoluta convoluta and Oxyposthia praedator (Turbellaria, Acoela). Hydrobiologia 132(1):189–193CrossRefGoogle Scholar
  16. Ehlers U (1992a) Dermonephridia--modified epidermal cells with a probable excretory function in Paratomella rubra (Acoela, Plathelminthes). Microfauna Mar 7:253–264Google Scholar
  17. Ehlers U (1992b) On the fine structure of Paratomella rubra Rieger & Ott (Acoela) and the position of the taxon Paratomella Dörjes in a phylogenetic system of the Acoelomorpha (Plathelminthes). Microfauna Mar 7:265–293Google Scholar
  18. Faubel A, Dörjes J (1978) Flagellophora apelti gen.N. sp.n.: a remarkable representative of the order Nemertodermatida (Turbellaria: Archoophora). Senckenb Marit 10:1–13Google Scholar
  19. Haszprunar G (2015) Review of data for a morphological look on Xenacoelomorpha (Bilateria incertae sedis). Org Divers Evol 16(2):363–389.  https://doi.org/10.1007/s13127-015-0249-z CrossRefGoogle Scholar
  20. Hejnol A (2015) Acoelomorpha and Xenoturbellida. In: Wanninger A (ed) Evolutionary developmental biology of invertebrates vol. 1. Springer, Vienna, pp 203–214CrossRefGoogle Scholar
  21. Hejnol A (2016) Acoelomorpha. In: Structure and evolution of invertebrate nervous systems. Andreas Schmidt-Rhaesa, Steffen Harzsch, Günter Purschke. Oxford University Press, Oxford, pp 56–62Google Scholar
  22. Hejnol A, Pang K (2016) Xenacoelomorpha’s significance for understanding bilaterian evolution. Curr Opin Genet Dev:48–54.  https://doi.org/10.1016/j.gde.2016.05.019
  23. Henry JQ, Martindale MQ, Boyer BC (2000) The unique developmental program of the acoel flatworm, Neochildia fusca. Dev Biol 220(2):285–295.  https://doi.org/10.1006/dbio.2000.9628 CrossRefGoogle Scholar
  24. Hooge M et al (2007) A revision of the systematics of panther worms (Hofstenia spp., Acoela), with notes on color variation and genetic variation within the genus. Hydrobiologia 592(1):439–454.  https://doi.org/10.1007/s10750-007-0789-0 CrossRefGoogle Scholar
  25. Israelsson O (1999) New light on the enigmatic Xenoturbella (phylum uncertain): ontogeny and phylogeny. Proc R Soc B Biol Sci 266:835.  https://doi.org/10.1098/rspb.1999.0713 CrossRefGoogle Scholar
  26. Israelsson O (2006) Observations on some unusual cell types in the enigmatic worm Xenoturbella (phylum uncertain). Tissue Cell 38(4):233–242.  https://doi.org/10.1016/j.tice.2006.05.002 CrossRefGoogle Scholar
  27. Israelsson O (2007) Chlamydial symbionts in the enigmatic Xenoturbella (Deuterostomia). J Invertebr Pathol 96(3):213–220.  https://doi.org/10.1016/j.jip.2007.05.002 CrossRefGoogle Scholar
  28. Ivanov AV, Mamkaev YV (1977) Über die Struktur des Digestionsparenchyms bei Turbellaria Acoela. Acta Zool Fenn 154:59–61Google Scholar
  29. Jennings JB (1957) Studies on feeding, digestion, and food storage in free-living flatworms (Platyhelminthes: Turbellaria). Biol Bull 112(1):63–80.  https://doi.org/10.2307/1538879 CrossRefGoogle Scholar
  30. Jondelius U, Wallberg A, Hooge M, Raikova OI (2011) How the worm got its pharynx: phylogeny, classification and bayesian assessment of character evolution in acoela. Syst Biol 60(6):845–871.  https://doi.org/10.1093/sysbio/syr073 CrossRefGoogle Scholar
  31. Karling T (1967) Zur Frage von dem systematischen Wert der Kategorien Archoophora und Neoophora (Turbellaria). Comment Biol Soc Sci Fenn 30(3):1–11Google Scholar
  32. Karling TG (1974) On the anatomy and affinities of the turbellarian orders. In: Riser NW, Morse MP (eds) Biology of the Turbellaria. McGraw-Hill, New York, pp 1–16Google Scholar
  33. Kjeldsen KU et al (2010) Two types of endosymbiotic bacteria in the enigmatic marine worm Xenoturbella bocki. Appl Environ Microbiol 76(8):2657–2662.  https://doi.org/10.1128/AEM.01092-09 CrossRefGoogle Scholar
  34. Klima J (1967) Zur Feinstrucktur des acoelen Süsswasserturbellars Oligochoerus limnophilus (Ax & Dörjes). Ver Naturwiss-Med Ver Innsb 55:107–124Google Scholar
  35. Kozloff EN (1972) Selection of food, feeding, and physical aspects of digestion in the Acoel Turbellarian Otocelis luteola. Trans Am Microsc Soc 91(4):556–565.  https://doi.org/10.2307/3225484 CrossRefGoogle Scholar
  36. Lundin K (2001) Degenerating epidermal cells in Xenoturbella (phylum uncertain), Nemertodermatida and Acoela (Platyhelminthes). Belg J Zool 131(1):153–157Google Scholar
  37. Lundin K, Hendelberg J (1996) Degenerating bodies ("pulsatile bodies") in the epidermis of Meara stichopi (Platyhelminthes, Nemertodermatida). Zoomorphology 116:1–5CrossRefGoogle Scholar
  38. Mamkaev YV (1967) ‘Ocherki po morfologii beskishechnykh turbellarij.’, Trudy Zool. Inst AN SSSR Leningrad 44:26–108Google Scholar
  39. Mamkaev YV (1986) Initial morphological diversity as a criterion in deciphering turbellarian phylogeny. Hydrobiologia 132:31–32CrossRefGoogle Scholar
  40. Mamkaev YV, Markosova TG (1982) Peculiarities of feeding and digestion of Oxyposthia praedator (Turbellaria, Acoela). Pacific Sci Cong Proceedings 14:97–102Google Scholar
  41. Mamkaev IV, Seravin LN (1963) Feeding of the acoelous turbellarian Convoluta convoluta (Abildgaard). J Zool Zh 47:197–205Google Scholar
  42. Markosova TG (1976) Acid phosphatase activity during digestion in the anintestinal Turbellaria Convoluta convoluta. Zh Evol Biokhim Fiziol 12:183–184Google Scholar
  43. Martinez P, Hartenstein V, Sprecher SG (2017) Xenacoelomorpha nervous systems. In: Sherman SM (ed) Oxford Encyclopaedia of neurosciences. Oxford University Press, OxfordGoogle Scholar
  44. Meyer-Wachsmuth I, Raikova OI, Jondelius U (2013) The muscular system of Nemertoderma westbladi and Meara stichopi (Nemertodermatida, Acoelomorpha). Zoomorphology 132(3):239–252.  https://doi.org/10.1007/s00435-013-0191-6 CrossRefGoogle Scholar
  45. Meyer-Wachsmuth I, Curini-Galletti M, Jondelius U (2014) Hyper-cryptic marine meiofauna: species complexes in Nemertodermatida. PLoS One 9(9):e107688.  https://doi.org/10.1371/journal.pone.0107688 CrossRefGoogle Scholar
  46. Papi F (1957) Sopra un nuovo Turbellario arcooforo di particolare significato filetico e sulla posizione della fam. Hofsteniidae nel sistema dei Turballari. Pubbl Stn Zool Napoli 30:132–148Google Scholar
  47. Pedersen KJ (1964) ‘the cellular organization of Convoluta convoluta, an acoels turbellarian: a cytological, histochemical and fine structural study'. Zeitschrift für Zellforschung und mikroskopische Anatomie (Vienna Austria, 1948) 64:655–687CrossRefGoogle Scholar
  48. Perea-Atienza E et al (2013) Posterior regeneration in Isodiametra pulchra (Acoela, Acoelomorpha). Front Zool 10(1):64.  https://doi.org/10.1186/1742-9994-10-64 CrossRefGoogle Scholar
  49. Philippe H et al (2011) Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470(7333):255–258.  https://doi.org/10.1038/nature09676 CrossRefGoogle Scholar
  50. Raikova OI (1987) Ultrastructural organization of the digestive system of the acoel turbellarian Actinoposthia beklemishevi Mamkaev. [in Russian]. Tr Zool Inst Nauk USSR 167:72–78Google Scholar
  51. Raikova OI et al (2000) An immunocytochemical and ultrastructural study of the nervous and muscular systems of Xenoturbella westbladi (Bilateria inc. sed.). Zoomorphology. 120(2):107–118.  https://doi.org/10.1007/s004350000028 CrossRefGoogle Scholar
  52. Ramachandra NB et al (2002) Embryonic development in the primitive bilaterian Neochildia fusca: normal morphogenesis and isolation of POU genes Brn-1 and Brn-3. Dev Genes Evol 212(2):55–69.  https://doi.org/10.1007/s00427-001-0207-y CrossRefGoogle Scholar
  53. Riedl R (1954) Neue Turbellarien aus dem mediterranen Felslittoral. Ergebnisse der “‘Unterwasser-Expedition Austria 1948– 1949’”. Zool Jahrb Syst (Wien) 82:157–244Google Scholar
  54. Riser NW (1987) Nemertinoides elongatus gen.N., sp.n. (Turbellaria: Nemertodermatida) from coarse sand beaches of the western North Atlantic. Proc Helmintol Soc Wash 54(1):60–67Google Scholar
  55. Rouse GW et al (2016) New deep-sea species of Xenoturbella and the position of Xenacoelomorpha. Nature. 530(7588):94–97.  https://doi.org/10.1038/nature16545 CrossRefGoogle Scholar
  56. Semmler H, Bailly X, Wanninger A (2008) Myogenesis in the basal bilaterian Symsagittifera roscoffensis (Acoela). Front Zool 5:1–15.  https://doi.org/10.1186/1742-9994-5-14 CrossRefGoogle Scholar
  57. Sikes JM, Bely AE (2008) Radical modification of the A-P axis and the evolution of asexual reproduction in Convolutriloba acoels. Evol Dev 10(5):619–631.  https://doi.org/10.1111/j.1525-142X.2008.00276.x CrossRefGoogle Scholar
  58. Smith JPS (1981) Fine-structural anatomy of the parenchyma in the Acoela and Nemertodermatida (Turbellaria). PhD. Thesis. North Carolina, Chapel HillGoogle Scholar
  59. Smith JPS III (1981) Fine-structural observations on the central parenchyma in Convoluta sp. Hydrobiologia 84:259–265CrossRefGoogle Scholar
  60. Smith J III, Tyler S (1985) The acoel turbellarians: kingpins of metazoan evolution or a specialized offshoot? In: Conway Morris S, George JD, Gibson R, Platt HM (eds) The origins and relationships of lower invertebrates. Clarendon Press, Oxford, p 123142Google Scholar
  61. Srivastava M et al (2014) Whole-body acoel regeneration is controlled by Wnt and bmp-Admp signaling. Curr Biol 24(10):1107–1113.  https://doi.org/10.1016/j.cub.2014.03.042 CrossRefGoogle Scholar
  62. Steinböck O (1930) Ergebnisse einer von E. Reisinger & 0. Steinbock mit Hilfe des Rask- 0rsted Fonds durchgefuhrten Reise in Gronland 1926.2. Nemertoderma buthycola nov. gen. nov. spec., eine eigenartige Turbellarie aus der Tiefe der Diskobay; nebst einem Beitrag zur Kenntnis des Nemertinenepithels. Vidensk Medd Dansk Nuturhist Foren 90:47–84Google Scholar
  63. Sterrer W (1998) New and known Nemertodermatida (Platyhelminthes-Acoelomorpha): a revision. Belgian J Zool 128(1):55–92Google Scholar
  64. Todt C (2009) Structure and evolution of the pharynx simplex in acoel flatworms (Acoela). J Morphol 270(3):271–290.  https://doi.org/10.1002/jmor.10682 CrossRefGoogle Scholar
  65. Tyler S, Rieger RM (1977) Ultrastructural evidence for the systematic position of the Nemertodermatida (Turbellaria). Acta Zool Fennica 54:193–207Google Scholar
  66. Westblad E (1940) Studien über skandinavische Turbellaria Acoela. Arkiv för Zoologi 32A(20):1–28Google Scholar
  67. Westblad E (1949a) On Meara stichopi (Bock) Westblad, a new representative of Turbellaria Archoophora. Ark Zool, Ser 2 1(5):43–57Google Scholar
  68. Westblad E (1949b) Xenoturbella bocki n.g., n. sp., a peculiar, primitive turbellarian type. Ark Zool 1:3–29Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Departament de Genètica, Microbiologia i EstadísticaUniversitat de BarcelonaBarcelonaSpain
  2. 2.Department of BiologyUniversity of FribourgFribourgSwitzerland
  3. 3.Department of BiologyUniversity of CaliforniaLos AngelesUSA
  4. 4.Institut Català de Recerca i Estudis Avançats (ICREA)BarcelonaSpain

Personalised recommendations