Put a tiger in your tank: The polyclad flatworm Maritigrella crozieri as a proposed model for evo-devo

EvoDevo

Volumn 4, Issue 1, 2013, Pages

  Lapraz, François ^a   Rawlinson, Kate A ^a,b   Girstmair, Johannes ^a,c   Tomiczek, Bartłomiej ^a   Berger, Jürgen ^d   Jékely, Gáspár ^d   Telford, Maximilian J ^a   Egger, Bernhard ^a,c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b DALHOUSIE UNIVERSITY   (Canada)

^c UNIVERSITY OF INNSBRUCK   (Austria)

^d MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

Evolutionary and developmental biology; Larvae; Neuropeptides; Planarians; Polyclad flatworms; Regeneration; Spiralians; Stem cells; Transcriptome; Turbellarians

Indexed keywords

ANIMALIA; LOPHOTROCHOZOA; MARITIGRELLA CROZIERI; PLATYHELMINTHES; POLYCLADIDA; SPIRALIA; TURBELLARIA;

EID: 84886741808     PISSN: None     EISSN: 20419139     Source Type: Journal    
DOI: 10.1186/2041-9139-4-29     Document Type: Review

References (99)

1. Rieger RM, Tyler S, Smith JPS, Rieger GE. Platyhelminthes: Turbellaria. Microscopic Anatomy of Invertebrates: Volume 3. Platyhelminthes Nemertinea 1991, 7-140. New York: Wiley-Liss, Harrison FW, Bogitsh BJ.
2. Egger B, Gschwentner R, Rieger R. Free-living flatworms under the knife: past and present. Dev Genes Evol 2007, 217:89-104. 10.1007/s00427-006-0120-5, 1784541, 17146688.
3. Philippe H, Brinkmann H, Copley RR, Moroz LL, Nakano H, Poustka AJ, Wallberg A, Peterson KJ, Telford MJ. Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 2011, 470:255-258. 10.1038/nature09676, 21307940.
4. Larsson K, Jondelius U. Phylogeny of Catenulida and support for Platyhelminthes. Org Divers Evol 2008, 8:378-387.
5. Giribet G. Assembling the lophotrochozoan (=spiralian) tree of life. Philos Trans R Soc Lond B Biol Sci 2008, 363:1513-1522. 10.1098/rstb.2007.2241, 2614230, 18192183.
6. Ehlers U. Das phylogenetische System der Plathelminthes 1985, Stuttgart, Germany: Gustav Fischer Verlag.
7. Littlewood DTJ. Platyhelminth systematics and the emergence of new characters. Parasite 2008, 15:333-341. 10.1051/parasite/2008153333, 18814704.
8. Martín-Durán JM, Egger B. Developmental diversity in free-living flatworms. EvoDevo 2012, 3:7. 10.1186/2041-9139-3-7, 3379954, 22429930.
9. Lockyer AE, Olson PD, Littlewood DTJ. Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biol J Linn Soc Lond 2003, 78:155-171.
10. Surface FM. The early development of a polyclad, Planocera Inquilina Wh. Proc Acad Nat Sci Phila 1907, 59:514-559.
11. Boyer BC, Henry JQ, Martindale MQ. Dual origins of mesoderm in a basal spiralian: cell lineage analyses in the polyclad turbellarian Hoploplana inquilina. Dev Biol 1996, 179:329-338. 10.1006/dbio.1996.0264, 8903349.
12. Rawlinson KA. Embryonic and post-embryonic development of the polyclad flatworm Maritigrella crozieri: implications for the evolution of spiralian life history traits. Front Zool 2010, 7:12. 10.1186/1742-9994-7-12, 2876153, 20426837.
13. Johnson KB, Forward RB. Larval photoresponses of the polyclad flatworm Maritigrella crozieri (Platyhelminthes, Polycladida) (Hyman). J Exp Mar Biol Ecol 2003, 282:103-112.
14. Scarpa J, Weis B, Ruppert E, Frick J, Ford A, Wright A. Direct evidence for planktotrophy in Müller's larva of the tiger flatworm, Pseudoceros crozieri [abstract]. Am Zool 1996, 36:107.
15. Rawlinson KA, Stella JS. Discovery of the corallivorous polyclad flatworm, Amakusaplana acroporae, on the Great Barrier Reef, Australia: the first report from the wild. PLoS One 2012, 7:e42240. 10.1371/journal.pone.0042240, 3411615, 22870308.
16. Bolaños DM. Comparative embryology and muscle development of polyclad flatworms (Platyhelminthes-Rhabditophorans). PhD thesis 2008, University of New Hampshire, Department of Zoology.
17. Selenka E. Zoologische Studien: 2 Zur Entwickelungsgeschichte der Seeplanarien 1881, Leipzig, Germany: W. Engelmann.
18. Anderson D. The embryonic and larval development of the turbellarian Notoplana australis (Schmarda, 1859) (Polycladida : Leptoplanidae). Mar Freshw Res 1977, 28:303-310.
19. Kato K. On the development of some Japanese polyclads. Jpn J Zool 1940, 8:537-573.
20. Wheeler W. Planocera inquilina, a polyclad inhabiting the branchial chamber of Syncotypus canaliculatus. Gill J Morphol 1894, 9:195-201.
21. Lang A. Die Polycladen (Seeplanarien) des Golfes von Neapel und der angrenzenden Meeresabschnitte: eine Monographie 1884, Leipzig, Germany: Verlag Wilhelm Engelmann.
22. Claparède T. Glanures zootomiques parmi les Annélides de Port Vendres (Pyrénées Orientales). Mémoires de la Société de Physique et d'Histoire Naturelle de Genève 1864, 17:463-600.
23. Remane A. Die Polycladen der Kieler Förde. Schriften Naturwiss Ver Schleswig-Holstein 1929, 19:73-79.
24. Younossi-Hartenstein A, Hartenstein V. The embryonic development of the polyclad flatworm Imogine mcgrathi. Dev Genes Evol 2000, 210:383-398. 10.1007/s004270000086, 11180845.
25. Galleni L. Polyclads of the Tuscan coasts. II. Stylochus alexandrinus Steinböck and Stylochus mediterraneus n. sp. from the rocky shores near Pisa and Livorno. Boll Zool 1976, 43:15-25.
26. Lytwyn MW, McDermott JJ. Incidence, reproduction and feeding of Stylochus zebra, a polyclad turbellarian symbiont of hermit crabs. Mar Biol 1976, 38:365-372.
27. Rawlinson KA, Bolaños DM, Liana MK, Litvaitis MK. Reproduction, development and parental care in two direct-developing flatworms (Platyhelminthes : Polycladida : Acotylea). J Nat Hist 2008, 42:2173-2192.
28. Hofker DJ. Faunistische Beobachtungen in der Zuidersee während der Trockenlegung. Z Für Morphol Ökologie Tiere 1930, 18:189-216.
29. Pearse AS, Wharton GW. The oyster " leech", Stylochus inimicus Palombi, associated with oysters on the coasts of Florida. Ecol Monogr 1938, 8:605-656.
30. Girard C. Researches upon Nemerteans and Planarians. I, Embryonic Development of Planocera Elliptica 1854, Philadelphia: Merrihew and Thompson.
31. Provenzano AJ. Effects of the flatworm Stylochus ellipticus (Girard) on oyster spat in two saltwater ponds in Massachusetts. Proc Natl Shellfish Assoc 1959, 50:83-88.
32. Müller J. Über verschiedene Formen von Seethieren. Arch Anat Physiol Wiss Med 1854, 69-98.
33. Gammoudi M, Noreña C, Tekaya S, Prantl V, Egger B. Insemination and embryonic development of some Mediterranean polyclad flatworms. Invertebr Reprod Dev 2012, 56:272-286.
34. Teshirogi W, Ishida S, Jatani K. On the early development of some Japanese polyclads. Rep Fukuara Mar Biol Lab 1981, 2-31.
35. Tang QY, Wang YJ, Wang XA. Early embryo and larva of Planocera reticulata: in vitro fertilization and SEM observation. Chin J Zool 2011, 46:66-71.
36. Faubel A. The Polycladida, Turbellaria: proposal and establishment of a new system. Part I. The Acotylea. Mitteilungen Aus Dem Hambg Zool Mus Inst 1983, 80:17-121.
37. Prudhoe S. A Monograph on Polyclad Turbellaria 1985, London: British Museum (Natural History).
38. Child CM. Studies on regulation. X. The positions and proportions of parts during regulation in Cestoplana in the absence of the cephalic ganglia. Arch Für Entwicklungsmechanik Org 1905, 20:157-186.
39. Tessmar-Raible K, Arendt D. Emerging systems: between vertebrates and arthropods, the Lophotrochozoa. Curr Opin Genet Dev 2003, 13:331-340. 10.1016/S0959-437X(03)00086-8, 12888005.
40. Newmark PA, Sánchez Alvarado A. Not your father's planarian: a classic model enters the era of functional genomics. Nat Rev Genet 2002, 3:210-219.
41. Crozier WJ. On the pigmentation of a polyclad. Proc Am Acad Arts Sci 1917, 52:725-730.
42. Hyman LH. Acoel and polyclad Turbellaria from Bermuda and the Sargassum. Bull Bingham Oceanogr Collect 1939, 7:Art. 1:1-26. 9 plates [Peabody Museum of Natural History, Yale University].
43. Newman LJ, Norenburg JL, Reed S. Taxonomic and biological observations on the tiger flatworm, Maritigrella crozieri (Hyman, 1939), new combination (Platyhelminthes, Polycladida, Euryleptidae) from Florida waters. J Nat Hist 2000, 34:799-808.
44. Newman LJ, Cannon LRG. A new genus of euryleptid flatworm (Platyhelminthes, Polycladida) from the Indo-Pacific. J Nat Hist 2000, 34:191-205.
45. Bolaños DM, Quiroga SY, Litvaitis MK. Five new species of cotylean flatworms (Platyhelminthes: Polycladida) from the wider Caribbean. Zootaxa 2007, 1650:1-23.
46. Litvaitis MK, Bolaños DM, Quiroga SY. When names are wrong and colours deceive: unravelling the Pseudoceros bicolor species complex (Turbellaria: Polycladida). J Nat Hist 2010, 44:829-845.
47. Bolaños DM, Litvaitis MK. Embryonic muscle development in direct and indirect developing marine flatworms (Platyhelminthes, Polycladida). Evol Dev 2009, 11:290-301. 10.1111/j.1525-142X.2009.00331.x, 19469856.
48. Boyer BC. Development of in vitro fertilized embryos of the polyclad flatworm, Hoploplana inquilina, following blastomere separation and deletion. Rouxs Arch Dev Biol 1987, 196:158-164.
49. Jékely G, Colombelli J, Hausen H, Guy K, Stelzer E, Nédélec F, Arendt D. Mechanism of phototaxis in marine zooplankton. Nature 2008, 456:395-399. 10.1038/nature07590, 19020621.
50. Meijering E, Dzyubachyk O, Smal I. Methods for cell and particle tracking. Methods Enzymol 2012, 504:183-200.
51. Gregory TR, Hebert PD, Kolasa J. Evolutionary implications of the relationship between genome size and body size in flatworms and copepods. Heredity (Edinb) 2000, 84:201-208. 10.1046/j.1365-2540.2000.00661.x, 10762390.
52. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29:644-652. 10.1038/nbt.1883, 3571712, 21572440.
53. Bortoluzzi S, d'Alessi F, Romualdi C, Danieli GA. The human adult skeletal muscle transcriptional profile reconstructed by a novel computational approach. Genome Res 2000, 10:344-349. 10.1101/gr.10.3.344, 311426, 10720575.
54. Dalyell JG. Observations on Some Interesting Phenomena in Animal Physiology 1814, Edinburgh, Archibald Constable: Exhibited by Several Species of Planariae. Illustrated by Coloured Figures of Living Animals.
55. Morgan TH. Experimental studies of the regeneration of Planaria maculata. Arch Für Entwicklungsmechanik Org 1898, 7:364-397.
56. Egger B, Ladurner P, Nimeth K, Gschwentner R, Rieger R. The regeneration capacity of the flatworm Macrostomum lignano--on repeated regeneration, rejuvenation, and the minimal size needed for regeneration. Dev Genes Evol 2006, 216:565-577. 10.1007/s00427-006-0069-4, 2441584, 16604349.
57. Olmsted JMD. The role of the nervous system in the regeneration of polyclad turbellaria. J Exp Zool 1922, 36:48-56.
58. Loeb J. Einleitung in die vergleichende Gehirnphysiologie und vergleichende Psychologie, mit besonderer Berücksichtigung der wirbellosen Thiere 1899, Leipzig, Germany: J. A. Barth.
59. Monti R. La Rigenerazione Nelle Planarie Marine 1900, Milan: Milan R. Istituto Lombardo.
60. Baguñà J, Romero R, Saló E, Collet J, Auladell C, Ribas M, Riutort M, García-Fernàndez J, Burgaya F, Bueno D. Growth, degrowth and regeneration as developmental phenomena in adult freshwater planarians. Exp Embryol Aquat Plants Anim 1990, 195:129-162. [NATO ASI Series A: Life Sciences. Edited by Marthy HJ.].
61. Wagner DE, Wang IE, Reddien PW. Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 2011, 332:811-816. 10.1126/science.1203983, 3338249, 21566185.
62. Egger B, Steinke D, Tarui H, De Mulder K, Arendt D, Borgonie G, Funayama N, Gschwentner R, Hartenstein V, Hobmayer B, Hooge M, Hrouda M, Ishida S, Kobayashi C, Kuales G, Nishimura O, Pfister D, Rieger R, Salvenmoser W, Smith J, Technau U, Tyler S, Agata K, Salzburger W, Ladurner P. To be or not to be a flatworm: the acoel controversy. PLoS One 2009, 4:e5502. 10.1371/journal.pone.0005502, 2676513, 19430533.
63. Drobysheva IM, Mamkaev YV. On mitosis in embryos and larvae of polyclads (Platyhelminthes). Belg J Zool 2001, 131:65-66.
64. Ladurner P, Egger B, Mulder K, Pfister D, Kuales G, Salvenmoser W, Schärer L. The stem cell system of the basal flatworm Macrostomum lignano. Stem Cells: From Hydra to Man 2008, 75-94. Dordrecht: Springer Netherlands, Bosch TCG.
65. Saló E, Baguñà J. Regeneration and pattern formation in planarians I. The pattern of mitosis in anterior and posterior regeneration in Dugesia (G) tigrina, and a new proposal for blastema formation. J Embryol Exp Morphol 1984, 83:63-80.
66. Egger B, Gschwentner R, Hess MW, Nimeth KT, Adamski Z, Willems M, Rieger R, Salvenmoser W. The caudal regeneration blastema is an accumulation of rapidly proliferating stem cells in the flatworm Macrostomum lignano. BMC Dev Biol 2009, 9:41. 10.1186/1471-213X-9-41, 2717932, 19604404.
67. Raff RA. Origins of the other metazoan body plans: the evolution of larval forms. Philos Trans R Soc Lond B Biol Sci 2008, 363:1473-1479. 10.1098/rstb.2007.2237, 2614227, 18192188.
68. Nielsen C. How did indirect development with planktotrophic larvae evolve?. Biol Bull 2009, 216:203-215.
69. Littlewood DTJ, Rohde K, Clough KA. The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biol J Linn Soc Lond 1999, 66:75-114.
70. Jägersten G. Evolution of the Metazoan Life Cycle: A Comprehensive Theory 1972, New York: Academic Press.
71. Nielsen C. Trochophora larvae: cell-lineages, ciliary bands and body regions. 2. Other groups and general discussion. J Exp Zool B Mol Dev Evol 2005, 304B:401-447.
72. Westheide W, Rieger R. Spezielle Zoologie. Teil 1: Einzeller und Wirbellose Tiere. 2. Auflage [Gebundene Ausgabe] 2006, Spektrum Akademischer Verlag: Heidelberg, Germany.
73. Martín-Durán JM, Romero R. Evolutionary implications of morphogenesis and molecular patterning of the blind gut in the planarian Schmidtea polychroa. Dev Biol 2011, 352:164-176. 10.1016/j.ydbio.2011.01.032, 21295562.
74. Saló E, Tauler J, Jimenez E, Bayascas JR, Gonzalez-Linares J, Garcia-Fernàndez J, Baguñà J. Hox and ParaHox genes in flatworms: characterization and expression. Am Zool 2001, 41:652-663.
75. Arendt D, Denes AS, Jékely G, Tessmar-Raible K. The evolution of nervous system centralization. Philos Trans R Soc Lond B Biol Sci 2008, 363:1523-1528. 10.1098/rstb.2007.2242, 2614231, 18192182.
76. Northcutt RG. Evolution of centralized nervous systems: two schools of evolutionary thought. Proc Natl Acad Sci USA 2012, 109(Suppl 1):10626-10633. 3386872, 22723354.
77. Denes AS, Jékely G, Steinmetz PRH, Raible F, Snyman H, Prud'homme B, Ferrier DEK, Balavoine G, Arendt D. Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 2007, 129:277-288. 10.1016/j.cell.2007.02.040, 17448990.
78. Nomaksteinsky M, Röttinger E, Dufour HD, Chettouh Z, Lowe CJ, Martindale MQ, Brunet JF. Centralization of the deuterostome nervous system predates chordates. Curr Biol 2009, 19:1264-1269. 10.1016/j.cub.2009.05.063, 19559615.
79. Hejnol A, Martindale MQ. Acoel development supports a simple planula-like urbilaterian. Philos Trans R Soc Lond B Biol Sci 2008, 363:1493-1501. 10.1098/rstb.2007.2239, 2614228, 18192185.
80. Nielsen C. Larval and adult brains. Evol Dev 2005, 7:483-489. 10.1111/j.1525-142X.2005.05051.x, 16174040.
81. Santagata S, Resh C, Hejnol A, Martindale MQ, Passamaneck YJ. Development of the larval anterior neurogenic domains of Terebratalia transversa (Brachiopoda) provides insights into the diversification of larval apical organs and the spiralian nervous system. EvoDevo 2012, 3:3. 10.1186/2041-9139-3-3, 3314550, 22273002.
82. Sinigaglia C, Busengdal H, Leclère L, Technau U, Rentzsch F. The bilaterian head patterning gene six3/6 controls aboral domain development in a cnidarian. PLoS Biol 2013, 11:e1001488. 10.1371/journal.pbio.1001488, 3586664, 23483856.
83. Hay-Schmidt A. The evolution of the serotonergic nervous system. Proc Biol Sci 2000, 267:1071-1079. 10.1098/rspb.2000.1111, 1690648, 10885511.
84. Dunn EF, Moy VN, Angerer LM, Angerer RC, Morris RL, Peterson KJ. Molecular paleoecology: using gene regulatory analysis to address the origins of complex life cycles in the late Precambrian. Evol Dev 2007, 9:10-24. 10.1111/j.1525-142X.2006.00134.x, 17227363.
85. Nielsen C. Animal Evolution: Interrelationships of the Living Phyla 2001, Oxford: Oxford University Press, 2.
86. Holland ND. Early central nervous system evolution: an era of skin brains?. Nat Rev Neurosci 2003, 4:617-627. 10.1038/nrn1175, 12894237.
87. Morris J, Cardona A, Del Mar De Miguel-Bonet M, Hartenstein V. Neurobiology of the basal platyhelminth Macrostomum lignano: map and digital 3D model of the juvenile brain neuropile. Dev Genes Evol 2007, 217:569-584. 10.1007/s00427-007-0166-z, 17611771.
88. Cebrià F. Organization of the nervous system in the model planarian Schmidtea mediterranea: an immunocytochemical study. Neurosci Res 2008, 61:375-384. 10.1016/j.neures.2008.04.005, 18499291.
89. Grimmelikhuijzen CJP, Hauser F. Mini-review: the evolution of neuropeptide signaling. Regul Pept 2012, 177(Suppl):S6-S9.
90. Conzelmann M, Offenburger SL, Asadulina A, Keller T, Münch TA, Jékely G. Neuropeptides regulate swimming depth of Platynereis larvae. Proc Natl Acad Sci USA 2011, 108:E1174-E1183. 10.1073/pnas.1109085108, 3219130, 22006315.
91. Conzelmann M, Williams EA, Tunaru S, Randel N, Shahidi R, Asadulina A, Berger J, Offermanns S, Jékely G. Conserved MIP receptor-ligand pair regulates Platynereis larval settlement. Proc Natl Acad Sci USA 2013, 110:8224-8229. 10.1073/pnas.1220285110, 3657792, 23569279.
92. Tomer R, Denes AS, Tessmar-Raible K, Arendt D. Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium. Cell 2010, 142:800-809. 10.1016/j.cell.2010.07.043, 20813265.
93. Asadulina A, Panzera A, Verasztó C, Liebig C, Jékely G. Whole-body gene expression pattern registration in Platynereis larvae. EvoDevo 2012, 3:27. 10.1186/2041-9139-3-27, 3586958, 23199348.
94. Menschaert G, Vandekerckhove TTM, Baggerman G, Landuyt B, Sweedler JV, Schoofs L, Luyten W, Van Criekinge W. A hybrid, de novo based, genome-wide database search approach applied to the sea urchin neuropeptidome. J Proteome Res 2010, 9:990-996. 10.1021/pr900885k, 2845465, 20000637.
95. Rowe ML, Elphick MR. The neuropeptide transcriptome of a model echinoderm, the sea urchin Strongylocentrotus purpuratus. Gen Comp Endocrinol 2012, 179:331-344. 10.1016/j.ygcen.2012.09.009, 23026496.
96. Mirabeau O, Joly JS. Molecular evolution of peptidergic signaling systems in bilaterians. Proc Natl Acad Sci USA 2013, 110:E2028-E2037. 10.1073/pnas.1219956110, 23671109.
97. Jékely G. Global view of the evolution and diversity of metazoan neuropeptide signaling. Proc Natl Acad Sci USA 2013, 110:8702-8707. 10.1073/pnas.1221833110, 3666674, 23637342.
98. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011, 7:539. 3261699, 21988835.
99. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. Jalview version 2: a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25:1189-1191. 10.1093/bioinformatics/btp033, 2672624, 19151095.