A new look at embryonic development of the visual system in decapod crustaceans: Neuropil formation, neurogenesis, and apoptotic cell death

Journal of Neurobiology

Volumn 39, Issue 2, 1999, Pages 294-306

  Harzsch, S ^a   Benton, J ^b   Dawirs, R R ^a   Beltz, B ^b  

^a BIELEFELD UNIVERSITY   (Germany)

^b WELLESLEY COLLEGE   (United States)

Author keywords

Apoptosis; Arthropod phylogeny; Crustacea; Neurogenesis; Visual system

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CRUSTACEA; EMBRYO; EMBRYO DEVELOPMENT; NERVOUS SYSTEM DEVELOPMENT; NEUROPIL; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; VISUAL SYSTEM;

ANIMALS; ANTIMETABOLITES; APOPTOSIS; BROMODEOXYURIDINE; FEMALE; GANGLIA, INVERTEBRATE; IN SITU NICK-END LABELING; NEPHROPIDAE; NEUROPIL; PHOTORECEPTORS, INVERTEBRATE; STEM CELLS; SYNAPSINS; TUBULIN; VISION; VISUAL PATHWAYS;

EID: 0032922929     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199905)39:2<294::AID-NEU13>3.0.CO;2-Q     Document Type: Article

References (71)

1. Ajiro K, Yoda K, Utsumi K, Nishikawa Y. 1996. Alteration of cell cycle dependent histone phosphorylation by okadais acid. J Biol Chem 271:13197-13201.
2. Akam M. 1998. The yin and yang of evo/devo. Cell 92: 153-155.
3. Anderson H. 1978. Postembryonic development of the visual system of the locust, Schistocerca gregaria: patterns of growth and developmental interactions in the retina and optic lobe. J Embryol Exp Morphol 45:55-83.
4. Anger K, Spivak E, Bas C, Ismael D, Luppi T. 1994. Hatching rhythms and dispersion of decapod crustean larvae in a brackish coastal lagoon in Argentina. Helgoländer Meeresuntersuch 48:445-466.
5. Averof M, Akam M. 1995. Insect-crustacean relationships: insights from comparative developmental and molecular studies. Phil Trans R Soc Lond B 347:293-303.
6. Bonini NM, Choi KW. 1995. Early decisions in Drosophila eye morphogenesis. Curr Opin Genet Dev 5:507-515.
7. Campos-Ortega JA. 1980. On compound eye development in Drosophila melanogaster. In: Hunt RK, editor. Current topics in developmental biology, 15. New York: Academic Press. p 347-371.
8. Cronin TW, Marshall NJ, Caldwell RL, Pales D. 1995. Compound eyes and ocular pigments of crustacean larvae (Stomatopoda and Decapoda, Brachyura). Mar Fresh Behav Physiol 26:219-231.
9. Cutforth T, Gaul U. 1997. The genetics of visual system development in Drosophila: specification, connectivity ansd asymmetry. Curr Opin Neurobiol 7:48-54.
10. Dohle W. 1997. Myriapod-insect relationships as opposed to an insect-crustacean sister group relationship. In: Fortey RA, Thomas RH, editors. Arthropod relationships. London: Chapman & Hall, p 305-315.
11. Dolbeare F. 1996. Bromodeoxyuridine: a diagnostic tool in biology and medicine. III. Proliferation in normal, injured and diseased tissue, growth factors, differentiation, DNA replication sites and in situ hybridization. Histochem J 28:531-575.
12. Douglass JK, Forward RB Jr. 1989. The ontogeny of facultative superposition optics in a shrimp eye: hatching through metamorphosis. Cell Tissue Res 258:289-300.
13. Eguchi E, Arikawa K, Ishibashi S, Suzuki T, Meyer-Rochow VB. 1989. Growth-related biometrical and biochemical studies of the compound eye of the crab, Hemigrapsus sanguineus. Zool Sci 6:241-250.
14. Elofsson R. 1969. The development of the compound eyes of Penaeus duorarum (Crustacea: Decapoda) with remarks on the nervous system. Z Zellforsch 97:323-350.
15. Elofsson R. 1992. To the question of eyes in primitive crustaceans. Acta Zool 73:369-372.
16. Elofsson R, Dahl E. 1970. The optic neuropils and chiasmata of crustacea. Z Zellforsch 107:343-360.
17. Elofsson R, Hagberg M. 1986. Evolutionary aspects on the construction of the first optic neuropil (lamina) in Crustacea. Zoomorphology 106:174-178.
18. Fincham AA. 1984. Ontogeny and optics of the eyes of the common prawn (Palaemon (Palaemon) serratus (Pennant, 1777). Zool J Linnean Soc 81:89-113.
19. Fincham AA. 1988. Ontogeny of anomuran eyes. Symp Zool Soc Lond 59:123-155.
20. Fischbach KF, Technau G. 1984. Cell degeneration in the developing optic lobes of the sine oculis and small-optic-lobes mutants of Drosophila melanogaster. Dev Biol 104:219-239.
21. Freeman M. 1997. Cell determination strategies in the Drosophila eye. Development 124:261-270.
22. Gaten E, Herring PJ. 1995. Morphology of the reflecting superposition eyes of larval ophlophorid shrimps. J Morphol 225:19-29.
23. Green P, Hartenstein AY, Hartenstein V. 1993. The embryonic development of the Drosophila visual system. Cell Tissue Res 273:583-598.
24. Hafner GS, Tokarski TR. 1998. Morphogenesis and pattern formation on the retina of the crayfish Procambarus clarkii. Cell Tissue Res 293:535-550.
25. Hafner GS, Tokarski T, Hammond-Soltis G. 1982. Development of the crayfish retina: a light and electron microscopic study. J Morphol 173:101-118.
26. Hafner GS, Tokarski TR, Kipp J. 1991. Changes in the microvillus cytoskeleton during rhabdom formation in the retina of the crayfish Procambarus clarkii. J Neurocytol 20:585-596.
27. Harzsch S, Anger K, Dawirs RR. 1997. Immunocytochemical detection of acetylated α-tubulin and Drosophila synapsin in the embryonic crustacean nervous system. Int J Dev Biol 41:477-484.
28. Harzsch S, Dawirs RR. 1994. Neurogenesis in larval stages of the spider crab Hyas araneus (Decapoda, Brachyura): proliferation of neuroblasts in the ventral nerve cord. Roux's Arch Dev Biol 204:93-100.
29. Harzsch S, Dawirs RR. 1995/96. Maturation of the compound eyes and eyestalk ganglia during larval development of the brachyuran crustaceans Hyas araneus L. (Decapoda, Majidae) and Carcinus maenas L. (Decapoda, Portunidae). Zoology 99:189-204.
30. Harzsch S, Dawirs RR. 1996. Neurogenesis in the developing crab brain: postembryonic generation of neurons persists beyond metamorphosis. J Neurobiol 29:384-398.
31. Harzsch S, Miller J, Benton J, Dawirs RR, Beltz BS. 1998a. Neurogenesis in the thoracic neuromeres of two crustaceans with different types of metamorphic development. J Exp Biol 201:2465-2479.
32. Harzsch S, Miller J, Benton J, Beltz BS. 1998b. From embryo to adult: persistent neurogenesis and apoptotic cell death shape the crustacean deutocerebrum. In: Elsner N, Wehner R, editors. Göttingen neurobiology report 1998. Stuttgart: Thieme. p 703.
33. Heberlein U, Moses K. 1995. Mechanisms of Drosophila retinal morphogenesis: the virtues of being progressive. Cell 81:987-990.
34. Helluy SM, Beltz BS. 1991. Embryonic development of the American lobster (Homarus americanus): quantitative staging and characterization of an embryonic molt cycle. Biol Bull 180:355-371.
35. Helluy SM, Ruchhoeft ML, Beltz BS. 1995. Development of the olfactory and accessory lobes in the American lobster: an allometric analysis and its implications for the deutocerebral structure of decapods. J Comp Neurol 357: 433-445.
36. Hofbauer A, Campos-Ortega JA. 1990. Proliferation pattern and early differentiation of the optic lobes in Drosophila melanogaster. Roux Arch Dev Biol 198:264-274.
37. Jacobson MD, Weil M, Raff MC. 1997. Programmed cell death in animal development. Cell 88:347-354.
38. Klagges BRE, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E. 1996. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154-3165.
39. Kraus O. 1997. Phylogenetic relationships between higher taxa of tracheate arthropods. In: Fortey RA, Thomas RH, editors. Arthropod relationships. London: Chapman & Hall, p 295-304.
40. Kukalova-Peck J. 1997. Arthropod phylogeny and "basal" morphological structures. In: Fortey RA, Thomas RH, editors. Arthropod relationships. London: Chapman & Hall. p 249-268.
41. Macagno ER, Lopresti V, Levinthal C. 1973. Structure and development of neural connections in isogenic organisms: variations and similarities in the optic system of Daphnia magna. Proc Natl Acad Sci Wash 79:57-61.
42. Malzacher P. 1968. Die Embryogenese des Gehirns paurometaboler Insekten. Untersuchungen an Carausius morosus und Periplaneta americana. Z Morph Tiere 62:103-161.
43. Martin AK, Poeckh B, Roth H, Ebens AJ, Ballard LC, Zipursky SL. 1995. Mutations disrupting neuronal connectivity in the Drosophila visual system. Neuron 14: 229-240.
44. Meinertzhagen IA. 1973. Development of the compound eye and optic lobes of insects. In: Young D, editor. Developmental neurobiology of arthropods. London: Cambridge University Press. p 51-104.
45. Meinertzhagen IA. 1993. Sleeping neuroblasts. Curr Biol 3:904-906.
46. Meinertzhagen IA, Hanson TE. 1993. The development of the optic lobe. In: Bate M, Martinez-Arias A, editors. The development of Drosophila melanogaster. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. p 1363-1491.
47. Meyer-Rochow VB. 1975. Larval and adult eye of the western rock lobster (Panulirus longipes). Cell Tissue Res 162:439-457.
48. Meyer-Rochow VB, Towers D, Ziedins I. 1990. Growth patterns in the eye of Petrolistes elongatus (Crustacea; Decapoda; Anomura). Exp Biol 48:329-340.
49. Mouze M. 1972. Croissance et metamorphose de l'appareil visuel des Aeschnidae (Odonata). Int J Insect Morphol Embryol 1:181-200.
50. Monsma SA, Booker R. 1996. Genesis of the adult retina and outer optic lobes of the moth, Manduca sexta. I. Patterns of proliferation and cell death. J Comp Neurol 367:10-20.
51. Nässel DR, Elofsson R, Odselius R. 1978. Neuronal connectivity in the compound of Artemia salina and Daphnia magna (Crustacea: Branchiopoda). Cell Tissue Res 190: 435-457.
52. Nilsson D-E. 1983. Evolutionary liks between apposition and superposition optics in crustacean eyes. Nature 302: 818-820.
53. Nilsson D-E. 1996. Old genes for new eyes. Curr Biol 6:39-42.
54. Nilsson D-E, Hallberg E, Elofsson R. 1986. The ontogenetic development of refracting superposition eyes in crustaceans: transformation of optical design. Tissue Cell 18: 509-519.
55. Nilsson D-E, Osorio D. 1997. Homology and parallelism in arthropod sensory processing. In: Fortey RA, Thomas RH, editors. Arthropod relationships. London: Chapman & Hall. p 333-348.
56. Negoescu A, Lorimier P, Labat-Moleur F, Drouet C, Robert C, Guillemet C, Brambilla C, Brambilla E. 1996. In situ apoptotic cell labeling by the TUNEL method: improvement and evaluation on cell preparations. J Histochem Cytochem 44:959-968.
57. Nordlander RH, Edwards JS. 1968. Morphological cell death in the post-embryonic development of the insect optic lobes. Nature 218:780-781.
58. Nordlander RH, Edwards JS. 1969. Postembryonic brain development in the monarch butterfly Danaus plexippus plexippus L. II. The optic lobe. Wilhelm Roux's Arch Entwicklungsmechanik Organismen 163:197-220.
59. Osorio D, Averof M, Bacon JP. 1995. Arthropod evolution: great brains, beautiful bodies. Trends Ecol Evol 10:449-454.
60. Petersen S. 1995. The embryonic development of Hyas araneus L. (Decapoda, Majidae): effects of temperature. Sarsia 80:193-198.
61. Petersen S, Anger K. 1997. Chemical and physiological changes during the embryonic development of the spider crab, Hyas araneus L. (Decapoda: Majidae). Comp Biochem Physiol 117B:299-306.
62. Sanders EJ, Wride MA. 1996. Ultrastructural identification of apoptotic nuclei using the TUNEL technique. Histochem J 28:275-281.
63. Scholtz G. 1997. Cleavage, germ band formation and head segmentation: the ground pattern of the Euarthropoda. In: Fortey RA, Thomas RH, editors. Arthropod relationships. London: Chapman & Hall. p 317-332.
64. Selleck SB, Gonzalez C, Glover DM, White K. 1992. Regulation of the G1-S transition in postembryonic neuronal precursors by axon ingrowth. Nature 355:253-255.
65. Wägele JW. 1993. Rejection of the "Uniramia" hypothesis and implications of the Mandibulata concept. Zool Jb Syst 120:253-288.
66. White E. 1996. Life, death, and the pursuit of apoptosis. Genes Dev 10:1-15.
67. Whitington PM, Bacon JP. 1997. The organization and development of the arthropod ventral nerve cord: insights into arthropod relationships. In: Fortey RA, Thomas RH, editors. Arthropod relationships. London: Chapman & Hall. p 349-370.
68. Williams TA, Nagy LM. 1996. Comparative limb development in insects and crustaceans. Semin Cell Dev Biol 7:615-628.
69. Wolff T, Ready DF. 1991. Cell death in normal and rough eye mutants of Drosophila. Development 113:825-839.
70. Wolff T, Ready DF. 1993. Pattern formation in the Drosophila retina. In: Bate M, Martinez-Arias, editors. The development of Drosophila melanogaster. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. p 1277-1325.
71. Wolff T, Martin KA, Rubin GM, Zipursky SL. 1997. The development of the Drosophila visual system. In: Cowan WM, Jessell TM, Zipursky SL, editors. Molecular and cellular approaches to neural development. New York: Oxford University Press. p 474-508.