Summary
Paedogenetically developing eggs of the gall midgeHeteropeza pygmaea are not deposited, but develop in the hemocoel of the mother larva. The nurse chamber remains present in the cleaving egg, and the follicular epithelium does not form a chorion but envelops the growing egg during embryonic development. It is possible to obtain “naked” eggs, i.e. eggs lacking the follicular epithelium, which are able to develop up to the blastoderm stage but remain spherical instead of assuming an elongated shape. Oogenesis of normal and naked eggs has been studied at the ultrastructural level with special reference to the nurse chamber. It is shown that the nurse chamber nuclei develop large nucleoli during oogenesis, indicating that the nurse chamber supplies the oocyte with ribosomal RNA (rRNA). The dense bodies in the nurse chamber may represent an intermediate stage in the transport of the rRNA from the nurse chamber to the oocyte; they are probably not related to the polar granules in the oocyte. It is also shown that the intercellular bridge joining the nurse chamber to the oocyte disappears shortly before cleavage initiation. During egg cleavage the follicular epithelium surrounds the nurse chamber, which degenerates and is gradually absorbed by the growing egg plasmodium. Naked cleaving eggs are never attached to a nurse chamber or to relics of it. Naked oocytenurse chamber complexes frequently aggregate, which may indicate a role of the follicular epithelium in follicle separation during normal development.
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References
Bier K (1963a) Synthese, interzellulärer Transport und Abbau von Ribonucleinsäure im Ovar der StubenfliegeMusca domestica. J Cell Biol 16:436–440
Bier K (1963b) Autoradiographische Untersuchungen über die Leistungen des Follikelepithels und der Nährzellen bei der Dotterbildung und Eiweißsynthese im Fliegenovar. Wilhelm Roux's Arch 154:552–575
Buvat R (1971) Origin and continuity of cell vacuoles. In: Reinert J, Ursprung H (eds) Origin and continuity of cell organelles. Springer, Berlin Heidelberg New York Tokyo, pp 127–158
Camenzind R (1966) Die Zytologie der bisexuellen und parthenogenetischen Fortpflanzung vonHeteropeza pygmaea Winnertz, einer Gallmücke mit pädogenetischer Vermehrung. Chromosoma 18:123–152
Camenzind R (1982) Das Follikelepithel während der paedogenetischen Entwicklung der GallmückeHeteropeza pygmaea (Cecidomyiidae, Diptera). Rev Suisse Zool 89:851–858
Choi WC, Nagl W (1977) Patterns of DNA and RNA synthesis during the development of ovarian nurse cells inGerris najas (Heteroptera) Dev Biol 61:262–272
Dapples CC, King RC (1970) The development of the nucleolus of the ovarian nurse cell ofDrosophila melanogaster. Z Zellforsch Mikrosk Anat 103:34–47
Fux T, Went DF, Camenzind R (1978) Movement pattern and ultrastructure of rotating follicles of the paedogenetic gall midgeHeteropeza pygmaea Winnertz (Diptera: Cecidomyiidae). Int J Insect Morphol Embryol 7:415–426
Hauschteck E (1962) Die Cytologie der Pädogenese und der Geschlechtsbestimmung einer heterogonen Gallmücke. Chromosoma 13:163–182
Ivanova-Kasas OM (1965) Trophic connections between the maternal organism and the embryo in paedogenetic Diptera (Cecidomyiidae). Acta Biol Hung 16:1–24
Junquera P (1983a) Polar plasm and pole cell formation in an insect egg developing with or without follicular epithelium: an ultrastructural study. J Exp Zool 227:441–452
Junquera P (1983b) The role of the follicular epithelium in growing eggs of a dipteran insect during late oogenesis and cleavage. J Morphol 178:303–312
Junquera P, Went DF (1981) A simple method enabling standardized handling of small biological objects for light and electron microscopic preparation. Experientia 37:534–535
Kunz W, Trepte HH, Bier K (1970) On the function of the germline chromosomes in the oogenesis ofWachtliella persicariae (Cecidomyiidae). Chromosoma 30:180–192
Lutz DA, Huebner E (1980) Development and cellular differentiation of an insect telotrophic ovary (Rhodnius prolixus). Tissue Cell 12:773–794
Madhavan MM (1973) The dual origin of the nurse chamber in the ovarioles of the gall midgeHeteropeza pygmaea. Wilhelm Roux's Arch 173:164–168
Mahowald AP (1971) Polar granules of Drosophila. III. The continuity of polar granules during the life cycle ofDrosophila. J Exp Zool 176:329–344
Mahowald AP (1975) Ultrastructural changes in the germ plasm during the life cycle ofMiastor (Cecidomyiidae, Diptera). Wilhelm Roux's Arch 176:223–240
Mahowald AP, Stoiber D (1974) The origin of the nurse chamber in ovarioles ofMiastor (Diptera: Cecidomyiidae). Wilhelm Roux's Arch 176:159–166
Meats M, Tucker JB (1976) Differentiation and positioning of nuclei in eggs of the cecidomydHeteropeza pygmaea. J Cell Sci 22:99–113
Meng C (1968) Strukturwandel und histochemische Befunde insbesondere am Oosom während der Oogenese und nach der Ablage des Eies vonPimpla turionella L. (Hymenoptera, Ichneumonidae). Wilhelm Roux's Arch 161:162–208
Panelius S (1968) Germ line and oogenesis during paedogenetic reproduction inHeteropeza pygmaea Winnertz (Diptera: Cecidomyiidae). Chromosoma 23:333–345
Schüpbach PM, Camenzind R (1983) Germ cell lineage and follicle formation in paedogenetic development ofMycophila speyeri Barnes (Diptera: Cecidomyiidae). Int J Insect Morphol Embryol 12:211–223
Schüpbach PM, Went DF (1983) Cell fusions during formation of the oocyte-nurse chamber complex in the ovary of the dipteran insectMycophila speyeri. Wilhelm Roux's Arch 192:228–233
Sitte P (1962) Einfaches Verfahren zur stufenlosen Gewebeentwässerung für die elektronenmikroskopische Präparation. Naturwissenschaften 17:402–403
Telfer WH (1975) Development and physiology of the oocyte-nurse cell syncytium. Adv Insect Physiol 11:223–319
Weissenfels N (1973) Lysosomen. In: Hirsch GC, Ruska H, Sitte P (eds) Grundlagen der Cytologie. Gustav Fischer Verlag, Jena, pp 297–303
Went DF (1971) In vitro culture of eggs and embryos of the viviparous paedogenetic gallmidgeHeteropeza pygmaea. J Exp Zool 177:301–312
Went DF (1972) Zeitrafferfilmanalyse der Embryonalentwicklung in vitro der vivipar paedogenetischen GallmückeHeteropeza pygmaea. Wilhelm Roux's Arch 170:13–47
Went DF (1974) Beziehungen zwischen Ovarkapazität, Mutterlarvenlänge und Nachkommenzahl bei der paedogenetischen GallmückeHeteropeza pygmaea (Dipt., Itonididae). Rev Suisse Zool 80:751–761
Went DF (1977a) In vitro culture of ovaries of a viviparous gall midge. In Vitro 13:76–84
Went DF (1977b) Pulsating oocytes and rotating follicles in an insect ovary. Dev Biol 55:392–396
Went DF, (1978) Oocyte maturation without follicular epithelium alters egg shape in a dipteran insect. J Exp Zool 205:149–155
Went DF, Junquera P (1981) Embryonic development of insect eggs formed without follicular epithelium. Dev Biol 86:100–110
Went DF, Fux T, Camenzind R (1978) Movement pattern and ultrastructure of pulsating oocyte nuclei of the paedogenetic gall midge,Heteropeza pygmaea (Winnertz (Diptera: Cecidomyiidae). Int J Insect Morphol Embryol 7:301–314
Zalokar M (1960) Sites of ribonucleic acid and protein synthesis inDrosophila. Exp Cell Res 19:184–196
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Junquera, P. Oogenesis in a paedogenetic dipteran insect under normal conditions and after experimental elimination of the follicular epithelium. Wilhelm Roux' Archiv 193, 197–204 (1984). https://doi.org/10.1007/BF01260339
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DOI: https://doi.org/10.1007/BF01260339