The urbilaterian brain revisited: Novel insights into old questions from new flatworm clades

Development Genes and Evolution

Volumn 223, Issue 3, 2013, Pages 149-157

  Bailly, Xavier ^a   Reichert, Heinrich ^b   Hartenstein, Volker ^c  

^a CNRS   (France)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acoel; Brain; Evolution; Platyhelminth; Urbilateria

Indexed keywords

ARTICLE; BRAIN; BRAIN DEVELOPMENT; BRAIN FUNCTION; CLADISTICS; COMPARATIVE STUDY; ELECTROENCEPHALOGRAM; EMBRYO; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM PARAMETERS; NEUROANATOMY; NONHUMAN; PHYLOGENY; PLATYHELMINTH; PRIORITY JOURNAL;

ANIMALS; BRAIN; PHYLOGENY; PLATYHELMINTHS;

ACOELOMORPHA; ANIMALIA; BILATERIA; PLATYHELMINTHES;

EID: 84876483414     PISSN: 0949944X     EISSN: 1432041X     Source Type: Journal    
DOI: 10.1007/s00427-012-0423-7     Document Type: Article

References (56)

1. Adoutte A, Balavoine G, Lartillot N (1999) Animal evolution: the end of the intermediate taxa? Trends Genet 15:104-108
2. Adoutte A, Balavoine G, Lartillot N, Lespinet O, Prud'homme B, De Rosa R (2000) The new animal phylogeny: reliability and implications. Proc Natl Acad Sci USA 97:4453-4456
3. Agata K, Soejima Y, Kato K, Kobayashi C, Umesono Y, Watanabe K (1998) Structure of the planarian central nervous system (CNS) revealed by neuronal cell markers. Zool Sci 15:433-440
4. Almuedo-Castillo M, Sureda-Gómez M, Adell T (2012) Wnt signaling in planarians: new answers to old questions. Int J Dev Biol 56(1-3):53-65
5. Arendt D, Denes AS, Jekely G, Tessmar-Raible K (2008) The evolution of nervous system centralization. Phil Trans R Soc Lond B 363:1523-1528
6. Barnes RSK, Calow P, Olive PJW (1993) The invertebrates. Blackwell, Oxford
7. Bery A, Cardona A, Martinez P, Hartenstein V (2010) Structure of the central nervous system of a juvenile acoel, Symsagittifera roscoffensis. Dev Genes Evol 220:61-76
8. Biserova NM (2000) The ultrastructure of glia-like cells in lateral nerve cords of adult Amphilina foliacea (Amphilinida). Acta Biol Hung 51(2-4):439-442
9. Biserova NM (2008) Do glial cells exist in the nervous system of parasitic and free-living flatworms? An ultrastructural and immunocytochemical investigation. Acta Biol Hung 59(Suppl):209-219
10. Boyan G, Loser M, Williams L, Liu Y (2011) Astrocyte-like glia associated with the embryonic development of the central complex in the grasshopper Schistocerca gregaria. Dev Genes Evol 221(3):141-155
11. Boyan GS, Liu Y, Loser M (2012) A cellular network of dye-coupled glia associated with the embryonic central complex in the grasshopper Schistocerca gregaria. Dev Genes Evol 222(3):125-138
12. Brindley PJ (2005) The molecular biology of schistosomes. Trends Parasitol 21(11):533-536
13. Brusca RC, Brusca GH (1990) Invertebrates. Sinauer, Sunderland
14. Bullock TH, Horridge GA (1965) Structure and function in the nervous system of invertebrates. Freeman, San Francisco
15. Cebria F (2008) Organization of the nervous system in the model planarian Schmidtea mediterranea: an immunocytochemical study. Neurosci Res 61:375-384
16. Delage Y (1886) Etudes histologiques sur le planaires rhabdocoeles acoleles (Convoluta schultzii O. Sch.). Arch Zool Exp Ben 4:109-144
17. Denes AS, Jekely G, Steinmetz PR, Raible F, Snyman H, Prud'homme B, Rerrier DE, Balavoine G, Arendt D (2007) Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129:277-288
18. Edgecombe GD, Giribet G, Dunn CW, Hejnol A, Kristensen RM, Neves RC, Rouse GW, WorsaaeetMartin K, Sørensen V (2011) Higher-level metazoan relationships: recent progress and remaining questions. Org Divers Evol 11(2):151-172
19. Gaerber CW, Salvenmoser W, Rieger RM, Gschwentner R (2007) The nervous system of Convolutriloba (Acoela) and its patterning during regeneration after sexual reproduction. Zoomorphology 126:73-87
20. Gustafsson MK, Halton DW, Kreshchenko ND, Movsessian SO, Raikova OI, Reuter M, Terenina NB (2002) Neuropeptides in flatworms. Peptides 23:2053-2061
21. Hanstroem B (1968) Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. Ascher, Amsterdam
22. Hartenstein V (2011) Morphological diversity and development of glia in Drosophila. Glia 59(9):1237-1252
23. Hartenstein V, Spindler S, Pereanu W, Fung S (2008) The development of the Drosophila larval brain. Adv Exp Med Biol 628:1-31
24. Hartline DK (2011) The evolutionary origins of glia. Glia 59(9):1215-1236
25. Hejnol A, Martindale MQ (2008) Acoel development supports a simple planula-like urbilaterian. Philos Trans R Soc Lond B Biol Sci 363(1496):1493-1501
26. Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguna J, Bailly X, Jondelius U, Wiens M, Müller WEG, Seaver E, Wheeler WE, Martindale MQ, Giribet G, Dunn CW (2009) Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc R Soc B 276:4261-4270
27. Hickman CP, Roberts LS, Larson A, l'Anson H (2004) Integrated principles of zoology. McGraw-Hill, New York
28. Holland LZ (2009) Chordate roots of the vertebrate nervous system: expanding the molecular toolkit. Nat Rev Neurosci 10:736-746
29. Hyman LH (1940) The invertebrates. McGraw-Hill, New York
30. Keenan CL, Coss R, Koopowitz H (1981) Cytoarchitectures of primitive brains: Golgi studies in flatworms. J Comp Neurol 195:697-716
31. Kotikova EA, Raikova OL (2008) Architectonics of the central nervous system of Acoela, Platyhelminthes, and Rotifera. J Evol Biochem Physiol 44:108
32. Lentz TL (1967) Fine structure of nerve cells in a planarian. J Morphol 121:323-337
33. Lichtneckert R, Reichert H (2005) Insights into the urbilaterian brain: conserved genetic patterning mechanisms in insect and vertebrate brain development. Heredity 94:465-477
34. Loverde PT, Osman A, Hinck A (2007) Schistosoma mansoni: TGF-beta signaling pathways. Exp Parasitol 117(3):304-317
35. Martín-Durán JM, Monjo F, Romero R (2012) Morphological and molecular development of the eyes during embryogenesis of the freshwater planarian Schmidtea polychroa. Dev Genes Evol 222(1):45-54
36. Morris J, Cardona A, De Miguel-Bonet Mdel M, Hartenstein V (2007) Neurobiology of the basal platyhelminth Macrostomum lignano: map and digital 3D model of the juvenile brain neuropile. Dev Genes Evol 217(8):569-584
37. Mwinyi A, Bailly X, Bourlat SJ, Jondelius U, Littlewood DTJ, Podsiadlowski L (2010) The phylogenetic position of Acoela as revealed by the complete mitochondrial genome of Symsagittifera roscoffensis. BMC Evol Biol 10:309
38. Nauta WJH, Fertag D (1986) Fundamental neuroanatomy. Freeman, San Francisco
39. Newmark PA, Wang Y, Chong T (2008) Germ cell specification and regeneration in planarians. Cold Spring Harb Symp Quant Biol 73:573-581
40. Peterson KJ, Eernisse DJ (2001) Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences. Evol Dev 3:170-205
41. Peterson KJ, Cotton JA, Gehling JG, Pisani D (2008) The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records. Phil Trans Soc B 363:1435-1443
42. Philippe H, Brinkmann H, Martinez P, Riutort M, Baguna J (2007) Acoel flatworms are not platyhelminthes: evidence from phylogenomics. PLoS One 2(8):e717
43. 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 470:255-258
44. Puelles L, Rubenstein JL (2003) Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 26:469-476
45. Ramachandra NB, Gates R, Ladurner P, Jacobs D, Hartenstein V (2002) Neurogenesis in the primitive bilaterian Neochildia I. Normal development and isolation of genes controlling neural fate. Dev Genes Evol 212:55-69
46. Reichert H (2009) Evolutionary conservation of mechanisms for neural regionalization, proliferation and interconnection in brain development. Biol Lett 5:112-116
47. Reisinger E (1925) Ein landbewohnender Archiannelide (Zugleich ein Beitrag zur Systematik der Archianneliden). Z MorpholÖkol Tiere 3:197-254
48. Reuter M, Gustafsson MKS (1995) The flatworm nervous system: pattern and phylogeny. In: Breidbach O, Kutsch W (eds) The nervous system of invertebrates. Birkhäuser, Basel
49. Reuter M, Raikova OI, Gustafsson MKS (1998) An endocrine brain? The pattern of FMRF-amide immunoreactivity in Acoela (Platyhelminthes). Tissue Cell 30:57-63
50. Riddiford N, Olson PD (2011) Wnt gene loss in flatworms. Dev Genes Evol 221(4):187-197
51. 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 52:701-713
52. von Graff L (1891) Die Organisation der Turbellaria Acoela. Leipzig
53. Wada H, Sato N (2001) Patterning the protochordate neural tube. Curr Opin Neurobiol 11:16-21
54. Wolpert L, Beddington R, Brockes J, Jessel T, Lawrence P, Meyerowitz E (1998) Principles of development. Oxford University Press, Oxford
55. Younossi-Hartenstein, A., Hartenstein, V. (2001) The embryonic development of the nervous system of the temnocephalid flatworms Craspedella pedum and Diceratocephala sp. Cell Tissue Res 204:295-310
56. Younossi-Hartenstein A, Ehlers U, Hartenstein V (2000) Embryonic development of the nervous system of the rhabdocoel flatworm Mesostoma lingua (Abildgaard, 1789). J Comp Neur 416:461-476