Advertisement

Xenacoelomorpha, a Key Group to Understand Bilaterian Evolution: Morphological and Molecular Perspectives

  • Ulf JondeliusEmail author
  • Olga I. RaikovaEmail author
  • Pedro MartinezEmail author
Chapter
First Online:

Abstract

The Xenacoelomorpha is a clade of mostly marine animals placed as the sister group of the remaining Bilateria (Nephrozoa) in most phylogenomic and morphological analyses, although alternative hypotheses placing them within deuterostomes have been proposed. This key phylogenetic position has raised recently a great interest in the study of their constitutive clades, since they can provide us with character states that illuminate different aspects of the origin of bilateral animals. Moreover, the recent availability of genomic and transcriptomic data from different species has been used in inferring the internal relationships among xenacoelomorph clades and the deciphering of molecular mechanisms that contribute to the evolution of metazoan genomes. Having access to molecular data paves the way to the systematic analysis of the genetic control of xenacoelomorph development and, additionally, to a better-informed study of bilaterian innovations. Here we revisit what has been learned over the last decades on the morphology, genomics and phylogenetic relationships of the Xenacoelomorpha.

This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

Funding from The Swedish Research Council (project 2018-05191) is gratefully acknowledged by Ulf Jondelius. The work of Olga Raikova was supported by the Ministry of Education and Science of the Russian Federation (project no. AAAA-A19-119020690076-7) and the RFBR (project numbers 16-04-00593a and 20-04-01006a). We would also like to thank Dr. Pierre Pontarotti (Marseille) for organizing the yearly “Evolutionary Biology Meeting” in Marseille and for inviting us to submit this chapter.

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. Frontiers Zool 9.  https://doi.org/10.1186/1742-9994-9-27CrossRefGoogle Scholar
  2. Achatz JG, Chiodin M, Salvenmoser W, Tyler S, Martinez P (2013) The Acoela: On Their Kind and Kinships, Especially with Nemertodermatids and Xenoturbellids (Bilateria Incertae Sedis). Org Diversity Evol 13(2):267–286.  https://doi.org/10.1007/s13127-012-0112-4CrossRefGoogle Scholar
  3. Andrikou C, Thiel D, Ruiz-Santiesteban JA, Hejnol A. (2019) Active mode of excretion across digestive tissues predates the origin of excretory organs. PLoS Biol 17(7):e3000408.  https://doi.org/10.1371/journal.pbio.3000408CrossRefGoogle Scholar
  4. Arboleda E, Hartenstein V, Martinez P, Reichert H, Sen S, Sprecher SG, Bailly X (2018) An emerging system to study photosymbiosis, brain regeneration, chronobiology, and behavior: the marine acoel symsagittifera roscoffensis. BioEssays 40(10).  https://doi.org/10.1002/bies.201800107CrossRefGoogle Scholar
  5. Arimoto A, Hikosaka-Katayama T, Hikosaka A, Tagawa K, Inoue T, Ueki T, Yoshida M et al (2019) A draft nuclear-genome assembly of the acoel flatworm Praesagittifera naikaiensis. GigaScience 8(4):1–8.  https://doi.org/10.1093/gigascience/giz023CrossRefGoogle Scholar
  6. Arroyo A, López-Escardó D, de Vargas C, Ruiz-Trillo I (2016) Hidden diversity of Acoelomorpha revealed through metabarcoding. Biol Lett 12(9).  https://doi.org/10.1098/rsbl.2016.0674CrossRefGoogle Scholar
  7. Bedini C, Ferrero E, Lanfranchi A (1973) The ultrastructure of ciliary sensory cells in two Turbellaria Acoela. Tissue Cell 5(3):359–372.  https://doi.org/10.1016/S0040-8166(73)80030-8CrossRefPubMedGoogle Scholar
  8. Beklemischev VN (1963) On the relationship of the Turbellaria to the other groups of the animal kingdom. In: Dougherty EC (ed) The lower Metazoa. University California Press, Berkeley, pp 234–244Google Scholar
  9. Bery A, Martínez P (2011) Acetylcholinesterase activity in the developing and regenerating nervous system of the acoel symsagittifera roscoffensis. Acta Zoologica 92(4):383–392.  https://doi.org/10.1111/j.1463-6395.2010.00472.xCrossRefGoogle Scholar
  10. Bery A, Cardona A, Martinez P, Hartenstein V (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/s00427-010-0328-2CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bleidorn C, Podsiadlowski L, Zhong M, Eeckhaut I, Hartmann S, Halanych KM, Tiedemann R (2009) On the phylogenetic position of Myzostomida: can 77 genes get it wrong? BMC Evol Biol 9(1):150CrossRefGoogle Scholar
  12. Boone M, Bert W, Claeys M, Houthoofd W, Artois T (2011) Spermatogenesis and the structure of the testes in Nemertodermatida. Zoomorphology 130:273–282CrossRefGoogle Scholar
  13. Børve A, Hejnol A (2014) Development and juvenile anatomy of the nemertodermatid Meara stichopi (Bock) Westblad 1949 (Acoelomorpha). Front Zool 11(January):50.  https://doi.org/10.1186/1742-9994-11-50CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bourlat SJ, Nielsen C, Lockyer AE, Littlewood DT, Telford MJ (2003) Xenoturbella is a deuterostome that eats molluscs. Nature 530:925–928CrossRefGoogle Scholar
  15. Bourlat SJ, Juliusdottir T, Lowe CJ, Freeman R, Aronowicz J, Kirschner M, Lander ES et al (2006) Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444(November):85–88.  https://doi.org/10.1038/nature05241CrossRefGoogle Scholar
  16. Brauchle M, Bilican A, Eyer C, Bailly X, Martínez P, Ladurner P, Bruggmann R, Sprecher SG (2018) Xenacoelomorpha survey reveals that all 11 animal Homeobox gene classes were present in the first Bilaterians. Genome Biol Evol 10(9):2205–2217.  https://doi.org/10.1093/gbe/evy170CrossRefPubMedPubMedCentralGoogle Scholar
  17. Buckland-Nicks J, Lundin K, Wallberg A (2018) The sperm of Xenacoelomorpha revisited: implications for the evolution of early Bilaterians. Zoomorphology.  https://doi.org/10.1007/s00435-018-0425-8CrossRefGoogle Scholar
  18. Cannon JT, Vellutini B, Smith J, Ronquist F, Jondelius U, Hejnol A (2016) Xenacoelomorpha is the sister group to Nephrozoa. Nature 530(7588):89–93.  https://doi.org/10.1038/nature16520CrossRefPubMedGoogle Scholar
  19. Chang YC, Pai CY, Chen YC, Ting HC, Martinez P, Telford MJ. Yu JK, Su YH (2015) Regulatory circuit rewiring and functional divergence of the duplicate admp genes in dorsoventral axial patterning.  https://doi.org/10.1016/j.ydbio.2015.12.015CrossRefGoogle Scholar
  20. Chiodin M, Achatz JG, Wanninger A, Martinez P (2011) Molecular architecture of muscles in an acoel and its evolutionary implications. J Exp Zool B Mol Dev Evol 316(6):427–439.  https://doi.org/10.1002/jez.b.21416CrossRefPubMedPubMedCentralGoogle Scholar
  21. Chiodin M, Børve A, Berezikov E, Ladurner P, Martinez P, Hejnol A (2013) Mesodermal gene expression in the acoel Isodiametra pulchra indicates a low number of mesodermal cell types and the endomesodermal origin of the gonads. PLoS ONE 8(2):e55499.  https://doi.org/10.1371/journal.pone.0055499CrossRefPubMedPubMedCentralGoogle Scholar
  22. Conway-Morris S, George JD, Gibson R, Pllatt HM (1985) The origins and relationships of lower invertebrates. Clarendon Press, OxfordGoogle Scholar
  23. Cook CE, Jimenez-Guri E, Akam M, Salo E (2004) The hox gene complement of acoel flatworms, a basal bilaterian clade. Article Evol Dev 6(3):154–163CrossRefGoogle Scholar
  24. Crezée M (1978) Paratomella rubra Rieger and Ott, an amphiatlantic acoel turbellarian. Cah Biol Mar 19:1–9Google Scholar
  25. Dittmann IL, Zauchner T, Nevard LM, Telford MJ, Egger B (2018) SALMFamide2 and serotonin immunoreactivity in the nervous system of some acoels (Xenacoelomorpha). J Morphol 279(5):589–597CrossRefGoogle Scholar
  26. Dorey AE (1965) The organization and replacement of the epidermis in acoelous turbellarians. Q J Microsc Sci 106:147–172PubMedGoogle Scholar
  27. Dörjes J (1968) Die Acoela (Turbellaria) Der Deutschen Nordseekste Und Ein Neues System Der Ordnung. Z. Zool Syst Evolutionforsch 6:56–452CrossRefGoogle Scholar
  28. Dörjes J (1972) Faerlea echinocardii Sp. N. Und Diskussion Der Gattungen Avagina Leiper Und Faerlea Westblad (Turbellaria Acoela). Zoolog Scr 1(3):185–189CrossRefGoogle Scholar
  29. Ehlers U (1984) Phylogenetisches system der plathelminthes. Verh Natwiss Ver Hamburg 27:291–294Google Scholar
  30. Ehlers U (1985) Das Phylogenetische System Der Plathelminthes. Gustav Fischer, StutgartGoogle Scholar
  31. Ehlers U (1991) Comparative morphology of statocysts in the Plathelminthes and the Xenoturbellida. Hydrobiologia 227:263–271CrossRefGoogle Scholar
  32. Ehlers U (1992a) Dermonephridia–modified epidermal cells with a probable excretory function in Paratomella rubra (Acoela, Plathelminthes). Microfauna Mar 7:253–64Google Scholar
  33. 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
  34. Ehlers U (1992c) Frontal glandular and sensory structures in Nemertoderma (Nemertodermatida) and Paratomella (Acoela): ultrastructure and phylogenetic implications for the monophyly of the Euplathelminthes (Plathelminthes). Zoomorphology 112(4):227–236.  https://doi.org/10.1007/BF01632820CrossRefGoogle Scholar
  35. Falleni A, Raikova O, Gremigni V (1995) Ultrastructural and cytochemical features of the ovary in Paratomella rubra (Platyhelminthes, Acoela). J Submicroscopical Cytol Pathol 27:511–523Google Scholar
  36. Ferrero E (1973) A fine structural analysis of the statocyst in Turbellaria Acoela. Zoologica Scripta 2(1):5–16.  https://doi.org/10.1111/j.1463-6409.1973.tb00793.xCrossRefGoogle Scholar
  37. Franzen A, Afzelius B (1987) The ciliated epidermis of Xenoturbella bocki (Platyhelminthes, Xenoturbellida) with some phylogenetic considerations. Zoolog Scr 16(1):9–17.  https://doi.org/10.1111/j.1463-6409.1987.tb00046.xCrossRefGoogle Scholar
  38. Gaerber CW, Salvenmoser W, Rieger RM, Gschwentner R (2007) The nervous system of Convolutriloba (Acoela) and its patterning during regeneration after asexual reproduction. Zoomorphology 126(2):73–87.  https://doi.org/10.1007/s00435-007-0039-zCrossRefGoogle Scholar
  39. Gavilán B, Sprecher SG, Hartenstein V, Martinez P (2019) The digestive system of xenacoelomorphs. Cell Tissue Res (in press).  https://doi.org/10.1007/s00441-019-03038-2CrossRefGoogle Scholar
  40. Gavilán B, Perea-Atienza E, Martínez P (2016) Xenacoelomorpha: a case of independent nervous system centralization? Philos Trans R Soc Lond S B Biol Sci 371(1685):20150039.  https://doi.org/10.1098/rstb.2015.0039CrossRefGoogle Scholar
  41. Gehrke AR, Neverett E, Luo Y-J, Brandt A, Ricci L, Hulett RE, Gompers A et al (2019) Acoel genome reveals the regulatory landscape of whole-body regeneration. Science 363 (6432):eaau6173.  https://doi.org/10.1126/science.aau6173CrossRefGoogle Scholar
  42. Graff LV (1905) Turbellaria I. Acoela. In: F Schulze (ed) Das Tierreich, Eine Zusammenstellung Und Kennzeichnung Der Rezenten Tierformen Heft 23, pp 23–34. Königl. Preuss. Akademie der Wissenschaften zu BerlinGoogle Scholar
  43. Graff LV (1911) Acoela, Rhabdocoela Und Alloeocoela Des Ostens Der Vereinigten Staaten von Amerika. Z Wiss Zool. 99:321–428Google Scholar
  44. Gröger H, Schmid V (2001) Larval development in Cnidaria: a connection to Bilateria? Genesis 29:110–114CrossRefGoogle Scholar
  45. Gschwentner R, Ladurner P, Nimeth K, Rieger R (2001) Stem cells in a basal bilaterian. S-phase and mitotic cells in Convolutriloba longifissura (Acoela, Platyhelminthes). Cell Tissue Res 304(3):401–408CrossRefGoogle Scholar
  46. Haszprunar G (2015) Review of data for a morphological look on Xenacoelomorpha (Bilateria Incertae Sedis). Org Diversity Evol 16(2):363–389.  https://doi.org/10.1007/s13127-015-0249-zCrossRefGoogle Scholar
  47. Hejnol A, Martindale MQ (2008) Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature 456(7220):382–386.  https://doi.org/10.1038/nature07309CrossRefPubMedGoogle Scholar
  48. Hejnol A, Martindale MQ (2009) Coordinated spatial and temporal expression of Hox genes during embryogenesis in the acoel Convolutriloba Longifissura. BMC Biol 1(7):65CrossRefGoogle Scholar
  49. Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P et al (2009) Assessing the root of bilaterian animals with scalable phylogenomic methods.  https://doi.org/10.1098/rspb.2009.0896CrossRefGoogle Scholar
  50. Hendelberg J (1969) On the development of different types of spermatozoa from spermatids with two flagella in the Turbellaria with remarks on the ultrastructure of the flagella. Zoologiska Bidrag Uppsala 38:1–52Google Scholar
  51. Hendelberg J (1977) Comparative morphology of turbellarian spermatozoa studied by electron microscopy. Acta Zoologica Fennica 154:149–162Google Scholar
  52. Hendelberg J (1986) The phylogenetic significance of sperm morphology in the Platyhelminthes. In: Advances in the biology of turbellarians and related platyhelminthes, pp 53–58. Springer, DordrechtCrossRefGoogle Scholar
  53. Hendelberg J, Hedlund K-O (1974) On the morphology of the epidermal ciliary rootlet system of the acoelous turbellarian Childia groenlandica. Zoon 2:13–24Google Scholar
  54. Hooge MD (2001) Evolution of the body-wall musculature in the Platyhelminthes (Acoelomorpha, Catenulida, Rhabditophora). J Morph 249:171–194CrossRefGoogle Scholar
  55. Iomini C, Raikova OI, Noury-Sraïri N, Justine J-L (1995) Immunocytochemistry of tubulin in spermatozoa of Platyhelminthes. Adv Spermatozoal Phylogeny Taxonomy 166:97–110Google Scholar
  56. Israelsson O (1997) Xenoturbella’s Molluscan Relatives…] and Molluscan Embryogenesis. Nature 390:32CrossRefGoogle Scholar
  57. Jondelius U, Ruiz-Trillo I, Baguñà J, Riutort M (2002) The Nemertodermatida are basal bilaterians and not members of the Platyhelminthes. Zool Scr 31(2):201–215.  https://doi.org/10.1046/j.1463-6409.2002.00090.xCrossRefGoogle Scholar
  58. 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/syr073CrossRefPubMedGoogle Scholar
  59. Kånneby T, Bernvi DC, Jondelius U (2015) Distribution, delimitation and description of species of Archaphanostoma (Acoela). Zool Scr 44(2):218–231.  https://doi.org/10.1111/zsc.12092CrossRefGoogle Scholar
  60. Karling TG (1940) Zur Morphologie Und Systematik Der Alloeocoela Cumulata and Rhabditophora Lecithophora (Turbellaria). Acta Zool Fennica 26:1–160Google Scholar
  61. Klauser MD, Smith JPS, Tyler S (1986) Ultrastructure of the frontal organ in Convoluta and Macrostomum spp.: significance for models of the turbellarian archetype. Hydrobiologia 132(1):47–52.  https://doi.org/10.1007/BF00046227CrossRefGoogle Scholar
  62. Lanfranchi A (1990) Ultrastructure of the epidermal eyespots of an acoel platyhelminth. Tissue Cell 22 (4):541–46. http://www.ncbi.nlm.nih.gov/pubmed/18620320CrossRefGoogle Scholar
  63. Lundin K (1997) Comparative ultrastructure of the epidermal ciliary rootlets and associated structures in species of the Nemertodermatida and Acoela (Plathelminthes). Zoomorphology 117 (2):81–92.  https://doi.org/10.1007/s004350050033CrossRefGoogle Scholar
  64. Lundin K (1998) The epidermal ciliary rootlets of Xenoturbella bocki (Xenoturbellida) revisited: new support for a possible kinship with the Acoelomorpha (Platyhelminthes). Zool Scr 27(3):263–270.  https://doi.org/10.1111/j.1463-6409.1998.tb00440.xCrossRefGoogle Scholar
  65. Lundin K, Hendelberg J (1998) Is the sperm type of the Nemertodermatida close to that of the ancestral Platyhelminthes? Hydrobiologia 383:197–205CrossRefGoogle Scholar
  66. Martín-Durán JM, Pang K, Børve A, Lê HS, Furu A, Cannon JT, Jondelius U, Hejnol A (2018) Convergent evolution of Bilaterian nerve cords. Nature 553(7686):45–50.  https://doi.org/10.1038/nature25030CrossRefGoogle Scholar
  67. Martinez P (2018) The Comparative method in biology and the essentialist trap. Frontiers in ecology and evolution 6 (AUG).  https://doi.org/10.3389/fevo.2018.00130
  68. Martinez P, Hartenstein V, Sprecher SG (2017) Xenacoelomorpha Nervous Systems. In: SM Sherman (ed) Oxford encyclopaedia of neurosciences. Oxford University PressGoogle Scholar
  69. Meyer-Wachsmuth I, Jondelius U (2016) Interrelationships of Nemertodermatida. Org Div Evol.  https://doi.org/10.1007/s13127-015-0240-8CrossRefGoogle Scholar
  70. 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/s00435-013-0191-6CrossRefGoogle Scholar
  71. 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.0107688CrossRefPubMedPubMedCentralGoogle Scholar
  72. Moreno E, De Mulder K, Salvenmoser W, Ladurner P, Martínez P (2010) Inferring the ancestral function of the posterior hox gene within the Bilateria: controlling the maintenance of reproductive structures, the musculature and the nervous system in the acoel flatworm Isodiametra pulchra. Evol Dev May.  https://doi.org/10.1111/j.1525-142x.2010.00411.xCrossRefGoogle Scholar
  73. Moreno E, Nadal M, Baguñà, J, Martínez P (2009) Tracking the origins of the Bilaterian hox patterning system: insights from the acoel flatworm Symsagittifera roscoffensis. Evol Dev 11 (5).  https://doi.org/10.1111/j.1525-142X.2009.00363.xCrossRefGoogle Scholar
  74. Mulder K De, Kuales G, Pfister D, Willems M, Egger B, Salvenmoser W, Thaler M et al (2009) Characterization of the stem cell system of the acoel Isodiametra pulchra. BMC Dev Biol 9:69.  https://doi.org/10.1186/1471-213X-9-69CrossRefPubMedPubMedCentralGoogle Scholar
  75. Mwinyi A, Bailly X, Bourlat SJ, Jondelius U, Littlewood TJ, Podsiadlowski L (2010) The phylogenetic position of Acoela as revealed by the complete mitochondrial genome of Symsagittifera roscoffensis. BMC Evol Biol 10:309.  https://doi.org/10.1186/1471-2148-10-309CrossRefPubMedPubMedCentralGoogle Scholar
  76. Nakano H, Miyazawa H, Maeno A, Shiroishi T, Kakui K, Koyanagi R, Kanda M, Satoh N, Omori A, Kohtsuka H (2017) A new species of Xenoturbella from the western Pacific Ocean and the evolution of Xenoturbella. BMC Evol Biol 17(1):245CrossRefGoogle Scholar
  77. Noren M, Jondelius U (1997) Xenoturbella’s molluscan relatives. Nature 390:31–32.  https://doi.org/10.1038/36242CrossRefGoogle Scholar
  78. Obst M, Nakano H, Bourlat SJ, Thorndyke MC, Telford MJ, Nyengaard JR, Funch P (2011) Spermatozoon ultrastructure of Xenoturbella bocki (Westblad 1949). Acta Zool 92(2):109–115.  https://doi.org/10.1111/j.1463-6395.2010.00496.xCrossRefGoogle Scholar
  79. Paps J, Holland PWH (2018) Reconstruction of the ancestral metazoan genome reveals an increase in genomic novelty. Nat Commun 9(1):1730.  https://doi.org/10.1038/s41467-018-04136-5CrossRefPubMedPubMedCentralGoogle Scholar
  80. Perea-Atienza E, Gavilán B, Chiodin M, Abril J-F, Hoff KJ, Poustka AJ, Martinez P (2015) The nervous system of Xenacoelomorpha: a genomic perspective. J Exp Biol 218(Pt 4):618–628.  https://doi.org/10.1242/jeb.110379CrossRefPubMedGoogle Scholar
  81. Perea-Atienza E, Sprecher SG, Martínez P (2018) Characterization of the bHLH family of transcriptional regulators in the acoel S. roscoffensis and their putative role in neurogenesis. Evodevo 9:8Google Scholar
  82. Petrov AA, Hooge M, Tyler S (2004) Ultrastructure of sperms in Acoela (Acoelomorpha) and its concordance with molecular systematics. Invertebr Biol 123:183–197CrossRefGoogle Scholar
  83. Philippe H, Brinkmann H, Copley RR, Moroz LL, Nakano H, Poustka AJ, Wallberg A, Peterson KJ, Telford MJ (2011) Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470(7333):255–258.  https://doi.org/10.1038/nature09676CrossRefPubMedPubMedCentralGoogle Scholar
  84. Philippe H, PoustkaAJ, Chiodin M, Hoff KJ, Dessimoz C, Tomiczek B, Schiffer PH, Müller S, Domman D, Horn M, Kuhl H, Timmermann B, Satoh N, Hikosaka-Katayama T, Nakano H, Rowe ML, Elphick MR, Thomas-Chollier M, Ha MJ (2019) Mitigating anticipated effects of systematic errors supports sister-group relationship between Xenacoelomorpha and Ambulacraria. Curr Biol (in press)Google Scholar
  85. Popova NV, Mamkaev YV (1985) Ultrastructure and primitive features of the eyes of Convoluta convoluta (Turbellaria Acoela). Dokl Akad Nauk SSSR 283:756–759Google Scholar
  86. Raikova OI (1991) On phylogenetic significance of ultrastructural characters in Turbellaria. In: Proceedings of the Zoological Institute of the Academy of Sciences of the USSR, pp 26–52Google Scholar
  87. Raikova OI (2004) Neuroanatomy of basal bilaterians (Xenoturbellida, Nemertodermatida, Acoela) and its phylogenetic implications (Ph.D. Thesis). Åbo Akademi University. Åbo, FinlandGoogle Scholar
  88. Raikova OI, Justine J-L (1999) Microtubular system during spermiogenesis and in the spermatozoon of Convoluta saliens (Platyhelminthes, Acoela): tubulin immunocytochemistry and electron microscopy. Mol Reprod Dev 52:74–85CrossRefGoogle Scholar
  89. Raikova OI, Falleni A, Gremigni V (1995) Oogenesis in Actinoposthia beklemischevi (Platyhelminthes, Acoela): an ultrastructural and cytochemical study. Tissue Cell 27:621–633CrossRefGoogle Scholar
  90. Raikova OI, Reuter M, Kotikova EA, Gustafsson MKS (1998) A commissural brain! The pattern of 5-HT immunoreactivity in Acoela (Plathelminthes). Zoomorphology 118(2):69–77.  https://doi.org/10.1007/s004350050058CrossRefGoogle Scholar
  91. Raikova OI, Reuter M, Jondelius U, Gustafsson MKS (2000a) An immunocytochemical and ultrastructural study of the nervous and muscular systems of Xenoturbella westbladi (Bilateria Inc. Sed.). Zoomorphology 120(2):107–18.  https://doi.org/10.1007/s004350000028CrossRefGoogle Scholar
  92. Raikova OI, Reuter M, Jondelius U, Gustafsson MKS (2000b) The brain of the Nemertodermatida (Platyhelminthes) as revealed by anti-5HT and anti-FMRFamide immunostainings. Tissue Cell 32(5):358–365.  https://doi.org/10.1054/tice.2000.0121CrossRefPubMedGoogle Scholar
  93. Raikova OI, Reuter M, Gustafsson MKS, Maule AG, Halton DW, Jondelius U (2004a) Basiepidermal nervous system in Nemertoderma westbladi (Nemertodermatida): GYIRFamide immunoreactivity. Zoology 107(1):75–86.  https://doi.org/10.1016/j.zool.2003.12.002CrossRefPubMedGoogle Scholar
  94. Raikova OI, Reuter M, Gustafsson MKS, Maule AG, Halton DW, Jondelius U (2004b) Evolution of the nervous system in Paraphanostoma (Acoela). Zool Scr 33:71–88CrossRefGoogle Scholar
  95. Raikova OI, Meyer-Wachsmuth I, Jondelius U (2016) The plastic nervous system of Nemertodermatida. Org Div Evol 16(1):85–104.  https://doi.org/10.1007/s13127-015-0248-0CrossRefGoogle Scholar
  96. Ramachandra NB, Gates RD, Ladurner P, Jacobs DK, Hartenstein V (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-yCrossRefPubMedGoogle Scholar
  97. Reisinger E (1925) Untersuchungen Am Nervensystem Der Bothrioplana semperi Braun. (Zugleich Ein Beitrag Zur Technik Der Vitalen Nervenfaerbung Und Zur Vergleichenden Anatomie Des Plathelminthennervensystem). Z Morphol Okol Tiere 5:119–149CrossRefGoogle Scholar
  98. Reisinger E (1960) Was ist Xenoturbella. Z Wiss Zool 164:188–198Google Scholar
  99. Reuter M, Raikova OI, Jondelius U, Gustafsson MKS, Maule AG, Halton, DV (2001) Organisation of the nervous system in the Acoela: an immunocytochemical study. Tissue Cell 33(2):119–28. http://www.ncbi.nlm.nih.gov/pubmed/11392663
  100. Reuter M, Raikova OI, Gustafsson MKS (2001) Patterns in the nervous and muscle systems in lower flatworms. Belgian J Zool 131 (Suppl:47–53Google Scholar
  101. Richter S, Loesel R, Purschke G, Schmidt-Rhaesa A, Scholtz G, Stach T, Vogt L, Wanninger A, Brenneis G, Döring C, Faller S, Fritsch M, Grobe P, Heuer CM, Kaul S, Møller OS, Müller CH, Rieger V, Rothe BH, Stegner ME, Harzsch S (2010) Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary. Front Zool. 7:29.  https://doi.org/10.1186/1742-9994-7-29CrossRefGoogle Scholar
  102. Rieger RM, Tyler S, Smith JPS III, Rieger GE (1991) Platyhelminthes: Turbellaria. In: Bogitsh BJ, Harrison FW (eds) Microscopic anatomy of invertebrates. Wiley-Liss, New YorkGoogle Scholar
  103. Robertson HE, Lapraz F, Egger B, Telford MJ, Schiffer PH (2017) The mitochondrial genomes of the acoelomorph worms Paratomella rubra, Isodiametra pulchra and Archaphanostoma ylvae. Sci R 7(1):1–16.  https://doi.org/10.1038/s41598-017-01608-4CrossRefGoogle Scholar
  104. Rohde K, Watson NA, Cannon LRG (1988) Ultrastructure of epidermal cilia of Pseudactinoposthia sp. (Platyhelminthes, Acoela); implications for the phylogenetic status of the Xenoturbellida and Acoelomorpha. J Submicroscopical Cytol Pathol 20:759–767Google Scholar
  105. Rouse GW, Wilson NG, Carvajal JI, Vrijenhoek RC (2016) New deep-sea species of Xenoturbella and the position of Xenacoelomorpha. Nature.  https://doi.org/10.1038/nature16545CrossRefPubMedGoogle Scholar
  106. Ruiz-Trillo I, Riutort M, Littlewood DT, Herniou EA, Baguña J (1999) Acoel flatworms: earliest extant bilaterian metazoans, not members of Platyhelminthes. Science 283 (5409):1919–23. http://www.ncbi.nlm.nih.gov/pubmed/10082465CrossRefGoogle Scholar
  107. Ruiz-Trillo I, Paps J, Loukota M, Ribera C, Jondelius U, Baguñà J, Riutort M (2002) A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemertodermatida are basal bilaterians. Proc Natl Acad Sci 99(17):11246–11251.  https://doi.org/10.1073/pnas.172390199CrossRefPubMedGoogle Scholar
  108. Ruiz-Trillo I, Riutort M, Fourcade HM, Baguñà J, Boore JL (2004) Mitochondrial genome data support the basal position of Acoelomorpha and the polyphyly of the Platyhelminthes. Mol Phylogenet Evol 33(2):321–332.  https://doi.org/10.1016/j.ympev.2004.06.002CrossRefPubMedGoogle Scholar
  109. Schmidt-Rhaesa, A. (2007). The evolution of organ systems. Oxford University PressGoogle Scholar
  110. Semmler H, Chiodin M, Bailly X, Martinez P, Wanninger A (2010) Steps towards a centralized nervous system in basal bilaterians: insights from neurogenesis of the acoel Symsagittifera roscoffensis. Dev Growth Differ 52(8):701–713.  https://doi.org/10.1111/j.1440-169X.2010.01207.xCrossRefPubMedGoogle Scholar
  111. Seo HC, Edvardsen RB, Maeland AD, Bjordal M, Jensen MF, Hansen A, Flaat M, Weissenbach J, Lehrach H, Wincker P, Reinhardt R, Chourrout D (2004) Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 431(7004):67–71CrossRefGoogle Scholar
  112. Sikes JM, Bely AE (2010) Making heads from tails: development of a reversed anterior–posterior axis during budding in an acoel. Dev Biol 338(1):86–97.  https://doi.org/10.1016/j.ydbio.2009.10.033CrossRefPubMedGoogle Scholar
  113. Smith III JPS, Tyler S (1988) Frontal organs in the Nemertodermatida (Turbellaria). Am Zool 28(4):140A, #747Google Scholar
  114. Smith III JPS, Tyler S, Rieger RM (1986) Is the Turbellaria Polyphyletic? Hydrobiologia 132:13–21CrossRefGoogle Scholar
  115. Smith JPS, Tyler S (1985) Fine-structure and evolutionary implications of the frontal organ in Turbellaria Acoela. 1 Diopisthoporus gymnopharyngeus sp.n. Zool Scr 14(2):91–102.  https://doi.org/10.1111/j.1463-6409.1985.tb00180.xCrossRefGoogle Scholar
  116. Smith JPS, Tyler S (1985) The acoel turbellarians: kingpins of metazoan evolution or a specialized offshoot?” In: Morris SC, George JD, Gibson R, Platt HM (eds) The origins and relationships of lower invertebrates, 123142. Oxford: Clarendon PressGoogle Scholar
  117. Sopott-Ehlers B, Ehlers U (1997) Ultrastructure of the subepidermal musculature of Xenoturbella bocki, the adelphotaxon of the Bilateria. Zoomorphology 117:71–79.  https://doi.org/10.1007/s004350050032CrossRefGoogle Scholar
  118. Sprecher SG, Bernardo-Garcia F-J, van Giesen L, Hartenstein V, Reichert H, Neves R, Bailly X et al. (2015) Functional brain regeneration in the acoel worm Symsagittifera roscoffensis. Biology Open 4 (12):1688–95.  https://doi.org/10.1242/bio.014266CrossRefGoogle Scholar
  119. Srivastava M, Mazza-Curll KL, van Wolfswinkel JC, Reddien PW (2014) Whole-body acoel regeneration is controlled by wnt and bmp-admp signaling. Curr Biol CB 24(10):1107–1113.  https://doi.org/10.1016/j.cub.2014.03.042CrossRefPubMedGoogle Scholar
  120. Sterrer W (1998) New and known Nemertodermatida (Platyhelminthes-Acoelomorpha): a revision. Belgian J Zool 128(1):55–92. https://www.researchgate.net/publication/265923621_New_and_known_Nemertodermatida_Platyhelminthes-Acoelomorpha_A_revision
  121. Tekle YI, Raikova OI, Justine J-L, Jondelius U (2007a) Ultrastructure and tubulin immunocytochemistry of the copulatory stylet-like structure in Childia species (Acoela). J Morphol 268:166–180CrossRefGoogle Scholar
  122. Tekle YI, Raikova OI, Justine J-L, Hendelberg J, Jondelius U (2007b) Ultrastructural and immunocytochemical investigation of acoel sperms with 9+ 1 axoneme structure: new sperm characters for unraveling phylogeny in Acoela. Zoomorphology 126:1–16CrossRefGoogle Scholar
  123. Telford MJ, Lockyer AE, Cartwright-Finch C, Littlewood TJ (2003) Combined large and small subunit ribosomal RNA phylogenies support a basal position of the acoelomorph flatworms. Proc Biol Sci 270 (1519):1077–83.  https://doi.org/10.1098/rspb.2003.2342CrossRefGoogle Scholar
  124. Thiel D, Franz-Wachtel M, Aguilera F, Hejnol A (2018) Xenacoelomorph neuropeptidomes reveal a major expansion of neuropeptide systems during early bilaterian evolution. Mol Biol Evol 35(10):2528–2543.  https://doi.org/10.1093/molbev/msy160CrossRefPubMedCentralGoogle Scholar
  125. 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.10682CrossRefPubMedGoogle Scholar
  126. Todt C, Tyler S (2006) Ciliary receptors associated with the mouth and pharynx of Acoela (Acoelomorpha): a comparative ultrastructural study. Acta Zoologica 88(1):41–58.  https://doi.org/10.1111/j.1463-6395.2007.00246.xCrossRefGoogle Scholar
  127. Tyler S (1979) Distinctive features of cilia in metazoans and their significance for systematics. Tissue Cell 11:385–400CrossRefGoogle Scholar
  128. Tyler S, Hooge MD (2004) Comparative morphology of the body wall in flatworms (Platyhelminthes). Can J Zool 82:194–210CrossRefGoogle Scholar
  129. Tyler S, Rieger RM (1975) Uniflagellate spermatozoa in Nemertoderma (Turbellaria) and their phylogenetic significance. Science 188:730–732CrossRefGoogle Scholar
  130. Tyler S, Rieger RM (1977) Ultrastructural evidence for the systematic position of the Nemertodermatida (Turbellaria). Acta Zool Fennica 54:193–207Google Scholar
  131. Uljanin WN (1870) Die Turbellarien Der Bucht von Sebastopol. Arbeiten Der 2.Versammlung Russischer Naturforscher Zu Moskau. 1869:1–96Google Scholar
  132. Westblad E (1937) Die Turbellarien-Gattung Nemertoderma Steinböck. Acta Societatis pro Fauna et Flora Fennica 60:45–89Google Scholar
  133. Westblad E (1940) Studien Über Skandinavische Turbellaria Acoela. I. Arkiv För Zoologi 32A(20):1–28Google Scholar
  134. Westblad E (1942) Studien Über Skandinavische Turbellaria Acoela. II. Arkiv För Zoologi 33A(14):1–48Google Scholar
  135. Westblad E (1945) Studien Über Skandinavische Turbellaria Acoela. III. Ark Zool. 36A(5):1–56Google Scholar
  136. Westblad E (1946) Studien Über Skandinavische Turbellaria Acoela. IV. Ark Zool 38A(1):1–56Google Scholar
  137. Westblad E (1948) Studien Über Skandinavische Turbellaria Acoela. V. Ark Zool 41:191–273Google Scholar
  138. Westblad E (1949a) On Meara stichopi (Bock) Westblad, a new representative of Turbellaria archoophora. Ark Zool Ser 2 1(5):43–57Google Scholar
  139. Westblad E (1949b) Xenoturbella bocki N.g., N. Sp., a peculiar, primitive Turbellarian type. Ark. Zool 1:3–29Google Scholar
  140. Yamasu T (1991) Fine structure and function of ocelli and sagittocysts of acoel flatworms. Hydrobiologia 227(1):273–282.  https://doi.org/10.1007/BF00027612CrossRefGoogle Scholar
  141. Zabotin YI (2019) Ultrastructure of epidermal sensillae in three species of Acoela. Invertebr Zool 6(1):71–77CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Swedish Museum of Natural HistoryStockholmSweden
  2. 2.Department of ZoologyStockholm UniversityStockholmSweden
  3. 3.Zoological Institute RASSt. PetersburgRussia
  4. 4.Faculty of Biology, Chair of Invertebrate ZoologySt. Petersburg State UniversitySt. PetersburgRussia
  5. 5.Department de Genètica, Microbiologia i EstadísticaUniversitat de BarcelonaBarcelonaSpain
  6. 6.ICREA (Institut Català de Recerca i Estudis Avancats)BarcelonaSpain

Personalised recommendations

Cite chapter

Buy options