Ovary structure and early oogenesis in the remipede, Godzilliognomus frondosus (Crustacea, Remipedia): Phylogenetic implications

Zoology

Volumn 115, Issue 4, 2012, Pages 261-269

  Kubrakiewicz, Janusz ^a   Jaglarz, Mariusz K ^b   Iliffe, Thomas M ^c   Bilinski, Szczepan M ^b   Koenemann, Stefan ^d  

^a UNIVERSITY OF WROC AW   (Poland)

^b JAGIELLONIAN UNIVERSITY   (Poland)

^c TEXAS A AND M UNIVERSITY AT GALVESTON   (United States)

^d UNIVERSITY OF SIEGEN   (Germany)

Author keywords

Crustacean evolution; Entognatha; Oogenesis; Ovary organization; Pancrustacea

Indexed keywords

ARTHROPODA; CEPHALOCARIDA; CRUSTACEA; GODZILLIOGNOMUS FRONDOSUS; HEXAPODA; ONYCHOPHORA; PANCRUSTACEA; REMIPEDIA;

EID: 84864051022     PISSN: 09442006     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.zool.2012.01.001     Document Type: Article

References (84)

1. Adiyodi R.G., Subramoniam T. Arthropoda - Crustacea. Reproductive Biology of Invertebrates 1983, vol. I:443-495. John Wiley & Sons, New York.
2. Ando H., Makioka T. Structure of the ovary and mode of oogenesis in a freshwater crayfish, Procambarus clarkia (Girard). Zool. Sci. 1998, 15:893-901.
3. Ando H., Makioka T. Structure of the ovary and mode of oogenesis in a freshwater crayfish, Potamon dehaani. J. Morphol. 1999, 239:107-114.
4. Andrew D.R. A new view of insect-crustacean relationships. II. Inferences from expressed sequence tags and comparisons with neural cladistics. Arthropod Struct. Dev. 2011, 40:289-302.
5. Ax P. Das System der Metazoa II. Ein Lehrbuch der phylogenetischen Systematik 1999, Gustav Fischer Verlag, Stuttgart.
6. Bertolani R. Tardigrada. Reproductive Biology of Invertebrates 1983, vol. I:431-443. John Wiley & Sons, New York.
7. Bilinski S. Structure of ovaries and oogenesis in entognathans (Apterygota). Int. J. Insect Morphol. Embryol. 1993, 22:255-269.
8. Bilinski S., Klag J. Gap junctions between oocyte and follicle cells in Acerentomon sp. (Insecta, Protura). Int. J. Invert. Reprod. 1982, 5:331-335.
9. Bilinski S., Hage W.J., Bluemink J.G. Gap junctions between the follicle cells and the oocyte during oogenesis in an insect, Tribolium destructor (Coleoptera). Roux's Arch. Dev. Biol. 1985, 194:296-300.
10. Blades-Eckelbarger P.I., Youngbluth M.J. The ultrastructure of oogenesis and yolk formation in Labidocera aestiva (Copepoda: Calanoida). J. Morphol. 1984, 179:33-46.
11. Boxshall G.A. On the anatomy of the misophrioid copepods, with special reference to Benthomisophria palliate Sars. Philos. Trans. R. Soc. Lond. B 1982, 297:125-181.
12. Boxshall G.A. Crustacean classification: on-going controversies and unresolved problems. Zootaxa 2007, 1668:313-325.
13. Brusca R.C., Brusca G.J. Invertebrates 2002, Sinauer Associates, Sunderland.
14. Buning J. The Insect Ovary: Ultrastructure Previtellogenic Growth and Evolution 1994, Chapman and Hall, London.
15. Buning J. The ovariole: structure, type and phylogeny. Microscopic Anatomy of Invertebrates, vol. 11C, Insecta 1998, 957-993. Wiley-Liss, New York. F.W. Harrison, M. Locke (Eds.).
16. Buning J. Ovariole structure supports sistergroup relationship of Neuropterida and Coleoptera. Arthropod Syst. Phyl. 2006, 64:115-126.
17. Carapelli A., Liò P., Nardi F., van de Wath E., Frati F. Phylogenetic analysis of mitochondrial protein coding genes confirms the reciprocal paraphyly of Hexapoda and Crustacea. BMC Evol. Biol. 2007, 7(Suppl. 2):S8.
18. Charniaux-Cotton H. Vitellogenesis and its control in malacostracan Crustacea. Am. Zool. 1985, 25:197-206.
19. Charniaux-Cotton H., Payen G. Crustacean reproduction. Endocrinology of Selected Invertebrate Types 1988, 279-303. Alan Liss, New York. H. Laufer, R.G.H. Downer (Eds.).
20. Criel G.R.J. Morphological study of the ovary of Artemia. Cell and Molecular Biology of Artemia Development 1989, 99-129. Plenum Press, New York. A.H. Warner, T.H. MacRae, J.C. Bagshaw (Eds.).
21. Dohle W. Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal of the proper name "Tetraconata" for the monophyletic unit Crustacea+Hexapoda. Origin of the Hexapoda 2001, vol. 37:85-103. Annales de la Société Entomologique de France (N.S.).
22. Ertas B., von Reumont B.M., Wagele J.W., Misof B., Burmester T. Hemocyanin suggests a close relationship of Remipedia and Hexapoda. Mol. Biol. Evol. 2009, 26:2711-2718.
23. Fanenbruck M., Harzsch S. A brain atlas of Godzilliognomus frondosus Yager, 1989 (Remipedia, Godzilliidae) and comparison with the brain of Speleonectes tulumensis Yager, 1987 (Remipedia, Speleonectidae): implications for arthropod relationships. Arthropod Struct. Dev. 2005, 34:343-378.
24. Fanenbruck M., Harzsch S., Wagele J.W. The brain of the Remipedia (Crustacea) and an alternative hypothesis on their phylogenetic relationships. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:3868-3873.
25. Giribet G., Edgecombe G.D., Wheeler W.C. Arthropod phylogeny based on eight molecular loci and morphology. Nature 2001, 413:157-161.
26. Harzsch S. Neurophylogeny: architecture of the nervous system and a fresh view on arthropod phylogeny. Integr. Comp. Biol. 2006, 46:162-194.
27. Hessler R.R., Elofsson R., Hessler A.Y. Reproductive system of Hutchinsoniella macracantha (Cepahlocarida). J. Crust. Biol. 1995, 15:493-522.
28. Hoef M.H.F., Dicus W.J.A.G., Hage W.J., Bluemink J.G. The ultrastructural organization of gap junctions between follicle cells and the oocyte in Xenopus laevis. Eur. J. Cell Biol. 1984, 33:242-247.
29. Ikuta K., Makioka T. Structure of the adult ovary and oogenesis in Argulus japonicus Thiele (Crustacea: Branchiura). J. Morphol. 1997, 231:29-39.
30. Ikuta K., Makioka T. Ovarian structure and oogenesis in the myodocopid ostracod, Vargula hilgendorfii. J. Crust. Biol. 1999, 19:730-737.
31. Ikuta K., Makioka T. Evolution of ovarian structure and oogenesis in maxillopodan crustaceans. Crustaceans and the Biodiversity Crisis 1999, 91-100. Leiden/Boston/Köln, Brill. F.R. Schram, J.C. von Vaupel Klien (Eds.).
32. Ikuta K., Maruo F., Tsutsumi T., Makioka T. Structure of the ovary and "nurse cells" in a freshwater ostracod Cyprinotus uenoi Brehm (Podocopida: Cypridoidea). Zool. Sci. 2007, 24:906-912.
33. Ito T. Origin of the basis in copepod limbs, with reference to the remipedian and cephalocarid limbs. J. Crust. Biol. 1989, 9:85-103.
34. Ito T., Schram F.R. Gonopores and the reproductive system of nectiopodan Remipedia. J. Crust. Biol. 1988, 8:250-253.
35. Jablonska A., Szklarzewicz T., Larink O., Bilinski S. Structure of ovaries in two collembolans, Allacma fusca and Arrhopalites coecus (Hexapoda, Entognatha). Fol. Histochem. Cytobiol. 1993, 31:87-92.
36. Jedrzejowska I., Kubrakiewicz J. The Balbiani body in the oocytes of a common cellar spider Pholcus phalangioides (Araneae: Pholcidae). Arthropod Struct. Dev. 2007, 36:317-326.
37. Jenner R.A. Higher-level crustacean phylogeny: consensus and conflicting hypotheses. Arthropod Struct. Dev. 2010, 39:143-153.
38. Jugan P., Zerbib C. Follicle cell tubular system in the prawn Macrobrachium rosenbergii: a route for exchanges between haemolymph and vitellogenic oocytes?. Biol. Cell. 1984, 51:395-398.
39. Kessel R.G., Tung H.N., Roberts R., Beams H.W. The presence and distribution of gap junctions in the oocyte-follicle cell complex of the zebrafish Brachydanio rerio. J. Submicrosc. Cytol. 1985, 17:239-253.
40. Koenemann S., Schram F.R., Bloechl A., Iliffe T.M., Hoenemann M., Held C. Post-embryonic development of remipede crustaceans. Evol. Dev. 2007, 9:117-121.
41. Koenemann S., Olesen J., Alwes F., Iliffe T.M., Hoenemann M., Ungerer P., Wolff C., Scholtz G. The post-embryonic development of Remipedia (Crustacea) - additional results and new insights. Dev. Genes Evol. 2009, 219:131-145.
42. Koenemann S., Jenner R.A., Hoenemann M., Stemme T., Reumont B.M. Arthropod phylogeny revisited, with a focus on crustacean relationships. Arthropod Struct. Dev. 2010, 39:88-110.
43. Krol R.M., Hawkins W.E., Overstreet R.M. Reproductive components. Microscopic Anatomy of Invertebrates Decapod Crustacea 1992, vol. 10:295-343. Wiley-Liss, New York.
44. Kubrakiewicz J. The ovary structure in two millipedes, Julus scandinavius and Orthomorpha gracilis (Myriapoda, Diplopoda). Zool. Poloniae 1987, 34:251-260.
45. Kubrakiewicz J. Ultrastructural investigation of the ovary structure of Ophyiulus pilosus (Myriapoda, Diplopoda). Zoomorphology 1991, 110:133-138.
46. Kubrakiewicz J., Klimowicz M. The ovary structure in Argulus foliaceus (Branchiura; Crustacea). Zool. Poloniae 1994, 39:7-14.
47. Makioka T. Ovarian structure and oogenesis in chelicerates and other arthropods. Proc. Arthropod. Embryol. Soc. Jpn. 1988, 23:1-11.
48. Matova N., Cooley L. Comparative aspects of animal oogenesis. Dev. Biol. 2001, 231:291-320.
49. Mayer G., Tait N.N. Position and development of oocytes in velvet worms shed light on the evolution of the ovary in Onychophora and Arthropoda. Zool. J. Linn. Soc. 2009, 157:17-33.
50. Miyazaki K., Bilinski S.M. Ultrastructural investigations of the ovary and oogenesis in the pycnogonids Cilunculus armatus and Ammothella biunguiculata (Pycnogonida, Ammotheidae). Invert. Biol. 2006, 125:346-533.
51. Miyazaki K., Makioka T. Structure of the adult reproductive system and oogenetic mode in the sea spider Endeis nodosa (Pycnogonida; Endeidae). J. Morphol. 1991, 209:257-263.
52. Miyazaki K., Makioka T. Adult female reproductive system and oogenesis in the sea spider Pycnogonum litorale (Pycnogonida; Pycnogomnnidae). Zool. Jb. Anat. 1992, 122:55-66.
53. Regier J.C., Shultz J.W. Elongation factor-2: a useful gene for arthropod phylogenetics. Mol. Phylog. Evol. 2001, 20:136-148.
54. Regier J.C., Shultz J.W., Kambic R.E. Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proc. R. Soc. Lond. B 2005, 272:395-401.
55. Regier J.C., Shultz J.W., Ganley A.R., Hussey A., Shi D., Ball B., Zwick A., Stajich J.E., Cummings M.P., Martin J.W., Cunningham C.W. Resolving arthropod phylogeny: exploring phylogenetic signal within 41kb of protein-coding nuclear gene sequence. Syst. Biol. 2008, 57:920-938.
56. Regier J.C., Shultz J.W., Zwick A., Hussey A., Ball B., Wetzer R., Cummings M.P., Martin J.W., Cunningham C.W. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 2010, 463:1079-1083.
57. Richter S. The Tetraconata concept: hexapod-crustacean relationships and the phylogeny of Crustacea. Org. Div. Evol. 2002, 2:217-237.
58. Richter S., Olsen J., Wheeler W.C. Phylogeny of Branchiopoda (Crustacea) based on combined analysis of morphological data and six molecular loci. Cladistics 2007, 23:301-336.
59. Richter S., Moller O.S., Wirkner C.S. Advances in crustacean phylogenetics. Arthropod Syst. Phyl. 2009, 67:275-286.
60. Rossi F. Comparative observations on the female reproductive system and parthenogenetic oogensis in Cladocera. Ital. J. Zool. 1980, 47:21-38.
61. Sareen M.L., Adiyodi K.G. Arthropoda - Myriapoda. Reproductive Biology of Invertebrates 1983, vol. I:497-519. Wiley and Sons, Chichester.
62. Schmitz E.H. Amphipoda. Microscopic Anatomy of Invertebrates Crustacea 1992, vol. 9:443-528. Wiley-Liss, New York.
63. Schram F.R. Crustacea 1986, Oxford University Press, Oxford.
64. Souty C. Electron microscopic study of follicle cell development during vitellogenesis in the marine crustacean Isopoda, Idotea balthica basteri. Reprod. Nutr. Dev. 1980, 20:653-663.
65. Spears T., Abele L.G. Crustacean phylogeny inferred from 18S rDNA. Arthropod Relationships 1997, 169-187. Chapman and Hall, London. R.A. Fortey, R.H. Thomas (Eds.).
66. Strausfeld N.J., Strausfeld C.M., Loesel R., Rowell D., Stowe S. Arthropod phylogeny: onychophoran brain organization suggests an archaic relationship with a chelicerate stem lineage. Proc. R. Soc. Lond. B 2006, 273:1857-1866.
67. Stys P., Bilinski S. Ovariole types and the phylogeny of hexapods. Biol. Rev. 1990, 65:401-429.
68. Stys P., Zrzavy J., Weyda F. Phylogeny of the Hexapoda and ovarian metamerism. Biol. Rev. 1993, 68:365-379.
69. Talbot P. The ovary of the lobster, Homarus americanus. I. Architecture of the mature ovary. J. Ultrastruct. Res. 1981, 76:235-248.
70. Tiegs O.W. The embryology and affinities of the Symphyla, based on a study of Hanseniella agilis. Q. J. Microsc. Sci. 1940, 82:1-225.
71. Tiegs O.W. The embryology and affinities of the Pauropoda, based on a study of Pauropus silvaticus. Q. J. Microsc. Sci. 1947, 88:165-267.
72. von Reumont, B.M., 2009. Molecular insights to crustacean phylogeny. Ph.D. Thesis. Rheinische Friedrich-Wilhelms-Universität, Bonn.
73. von Reumont B.M., Meusemann K., Szucsich N.U., Dell'Ampio E., Gowri-Shankar V., Bartel D., Simon S., Letsch H.O., Stocsits R.R., Luan Y., Wägele J.W., Pass G., Hadrys H., Misof B. Can comprehensive background knowledge be incorporated into substitution models to improve phylogenetic analysis?. A case study on major arthropod relationships. BMC Evol. Biol. 2009, 9:119. 10.1186/1471-2148-9-119.
74. von Reumont B.M., Jenner R.A., Wills M.A., Dell'Ampio E., Pass G., Ebersberger I., Meyer B., Koenemann S., Iliffe T.M., Stamatakis A., Niehuis O., Meusemann K., Misof B. Pancrustacean phylogeny in the light of new phylogenomic data: support for Remipedia as the possible sister group of Hexapoda. Mol. Biol. Evol. 2012, 29:1031-1045. 10.1093/molbev/msr270.
75. Wagele J.-W. Isopoda. Microscopic Anatomy of Invertebrates Crustacea 1992, vol. 9:529-617. Wiley-Liss, New York.
76. Walldorf V., Riehl R. Oogenesis in the pentastomid Raillietiella aegypti (Cephalobaenida). I. Previtellogenic and vitellogenic stages. Z. Parasitenk. 1985, 71:113-124.
77. Wheeler W.C., Giribet G., Edgecombe G.D. Arthropod systematics. The comparative study of genomic, anatomical and paleontological information. Assembling the Tree of Life 2004, 281-295. Oxford University Press, New York. J. Cracraft, M.J. Donoghue (Eds.).
78. Wills M.A. A phylogeny of recent and fossil Crustacea derived from morphological characters. Arthropod Relationships. The Systematics Association Special Volume Series 55 1997, 189-209. Chapman and Hall, London.
79. Yager J. Remipedia, a new class of Crustacea from a marine cave in the Bahamas. J. Crust. Biol. 1981, 1:328-333.
80. Yager J. The male reproductive system, sperm, and spermatophores of the primitive, hermaphroditic, remipede crustacean Speleonectes benjamini. Invert. Reprod. Dev. 1989, 15:75-81.
81. Yager J. The reproductive biology of two species of remipedes. Crustacean Sexual Biology 1991, 271-289. Columbia University Press, New York. R.T. Bauer, J.W. Martin (Eds.).
82. Zerbib C. Ultrastructural observation of oogenesis in the crustacea amphipoda Orchestia gammarellus (Pallas). Tissue & Cell 1980, 12:47-62.
83. Zerbib C., Jugan P. Mise en evidence d'un mode nouveau de franchissement de l'epithelium folliculaire secondaire chez le Crustace Decapode Macrobrachium rosenbergii. Int. J. Invert. Reprod. Dev. 1984, 7:227-235.
84. Zrzavy J., Stys P. The basic body plan of arthropods: insights from the evolutionary morphology and developmental biology. J. Evol. Biol. 1997, 10:353-367.