Skip to main content
Log in

Segmental organisation of the head in the embryo of Drosophila melanogaster

A blastoderm fate map of the cuticle structures of the larval head

  • Published:
Roux's archives of developmental biology Aims and scope Submit manuscript

Summary

Embryos of Drosophila melanogaster were irradiated in the presumptive head region with a UV-laser microbeam of 20 μm diameter at two developmental stages, the cellular blastoderm and the extended germ band. The ensuing defects were scored in the cuticle pattern of the head of the first-instar larva, which is described in detail in this paper. The defects caused by irradiating germ band embryos when morphologically recognisable lobes appear in the head region were used to establish the segmental origin of various head structures. This information enabled us to translate the spatial distribution of blastoderm defects into a fate map of segment anlagen. The gnathal segments derive from a region of the blastoderm between 60% and 70% egg length (EL) dorsally and 60% and 80% ventrally. The area anterior to the mandibular anlage and posterior to the stomodaeum is occupied by the small anlagen of the intercalary and antennal segments ventrally and dorsally, respectively. The labrum, which originates from a paired anlage dorsally at 90% EL, is separated from the remaining head segments by an area for which we did not observe cuticle defects following blastoderm irradiation, presumably because those cells give rise to the brain. The dorsal and lateral parts of the cephalo-pharyngeal skeleton appear to be the only cuticle derivatives of the non-segmental acron. These structures derive from a dorso-lateral area just behind the putative brain anlage and may overlap the latter. In addition to the segment anlagen, the regions of the presumptive dorsal pouch, anterior lobe and post-oral epithelium, whose morphogenetic movements during head involution result in the characteristic acephalic appearance of the larva, have been projected onto the blastoderm fate map. The results suggest that initially the head of the Drosophila embryo does not differ substantially from the generalised insect head as judged by comparison of fate map and segmental organisation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Behan M, Ryan MF (1978) Ultrastructure of antennal sensory receptors of Tribolium larvae (Coleoptera: Tenebrionidae). Int J Insect Morphol Embryol 7:221–236

    Google Scholar 

  • Bryant PJ (1978) Pattern formation in imaginal discs. In: Ashburner M, Wright TRF (eds) The genetics and biology of Drosophila, vol 2c. Academic Press, London, New York, San Francisco

    Google Scholar 

  • Chu-Wang I-W, Axtell RC (1972) Fine structure of the terminal organ of the house fly larva, Musca domestica L. Z Zellforsch 127:287–305

    Google Scholar 

  • Cook EF (1949) The evolution of the head in the larvae of the Diptera. Microentomology 14:1–57

    Google Scholar 

  • Eassa YEE (1953) The development of the imaginal buds in the head of Pieris brassicae Linn. (Lepidoptera). Trans R Ent Soc (Lond) 104:39–50

    Google Scholar 

  • Frederick RD, Denell RE (1982) Embryological origin of the antenno-maxillary complex of the larva of Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 11:227–233

    Google Scholar 

  • Gehring WJ, Seippel S (1967) Die Imaginalzellen des Clypeo-Labrums und die Bildung des Rüssels von Drosophila melanogaster. Rev Suisse Zool 74:589–596

    Google Scholar 

  • Haget A (1955) Experiences mettant en evidence l'origine paire du labre chez l'embryon du Coleoptere Leptinotarsa. CR Séances Soc Biol 149:690–692

    Google Scholar 

  • Hartenstein V, Campos-Ortega JA (1985) Fate-mapping in wild-type Drosophila melanogaster. I. The spatio-temporal pattern of embryonic cell divisions. Wilhelm Roux's Arch 194:181–195

    Google Scholar 

  • Hartenstein V, Technau GM, Campos-Ortega JA (1985) Fate-mapping in wild-type Drosophila melanogaster. III. A fate map of the blastoderm. Wilhelm Roux's Arch 194:213–216

    Google Scholar 

  • Hennig W (1948–52) Die Larvenformen der Dipteren. Akademie-Verlag, Berlin

    Google Scholar 

  • Hertweck H (1931) Anatomie und Variabilität des Nervensystems und der Sinnesorgane von Drosophila melanogaster Meigen. Z Wiss Zool 139:559–663

    Google Scholar 

  • Janning W (1978) Gynandromorph fate maps in Drosophila. In: Gehring W (ed) Genetic mosaics and cell differentiation (Results and problems in cell differentiation, vol 9). Springer, Berlin Heidelberg New York

    Google Scholar 

  • Keilin D (1915–6) Recherches sur les larves de Dipteres Cyclorraphes. Bull Sci Fr Belg 49:15–198

    Google Scholar 

  • Kobayashi Y, Ando H (1983) Embryonic development of the alimentary canal and ectodermal derivatives in the primitive moth, Neomicropteryx nipponensis Issiki (Lepidoptera, Micropterygidae). J Morphol 176:289–314

    Google Scholar 

  • Kobayashi Y, Ando H (1984) Mesodermal organogenesis in the embryo of the primitive moth, Neomicropteryx nipponensis Issiki (Lepidoptera, Micropterygidae). J Morphol 181:29–47

    Google Scholar 

  • Lawrence PA (1981) The cellular basis of segmentation in insects. Cell 26:3–10

    Google Scholar 

  • Lohs-Schardin M, Sander K, Cremer C, Cremer T, Zorn C (1979a) Localized ultraviolet laser microbeam irradiation of early Drosophila embryos: Fate maps based on location and frequency of adult defects. Dev Biol 68:533–545

    Google Scholar 

  • Lohs-Schardin M, Cremer C, Nüsslein-Volhard C (1979b) A fate map for the larval epidermis of Drosophila melanogaster: Localized cuticle defects following irradiation of the blastoderm with an ultraviolet laser microbeam. Dev Biol 73:239–255

    Google Scholar 

  • Matsuda R (1965) Morphology and evolution of the insect head. Mem Am Ent Inst 4:1–334

    Google Scholar 

  • Miall LC, Hammond AR (1892) The development of the head of the imago of Chironomus. Trans Linn Soc (Ser 2) Zool 5:265–279

    Google Scholar 

  • Morata G, Lawrence PA (1979) Development of the eye-antenna imaginai disc of Drosophila. Dev Biol 70:355–371

    Google Scholar 

  • Moulins M (1971a) La cavite preorale de Blabera craniifer Burm. (Insecte, Dictyoptere) et son innervation: etude anatomo-histologique de l'epipharynx et l'hypopharynx. Zool Jb Anat 88:527–586

    Google Scholar 

  • Moulins M (1971b) Ultrastructure et physiologie des organes epipharyngiens et hypopharyngiens (chimiorecepteurs cibariaux) de Blabera craniifer Burm. (Insecte, Dictyoptere). Z Vergl Physiol 73:139–166

    Google Scholar 

  • Poulson DF (1950) Histogenesis, organogenesis, and differentiation in the embryo of Drosophila melanogaster Meigen. In: Demerec M (ed) Biology of Drosophila. Wiley, New York

    Google Scholar 

  • Rempel JG (1975) The evolution of the insect head: the endless dispute. Quaest Entomol 11:7–25

    Google Scholar 

  • Rempel JG, Church NS (1971) The embryology of Lytta viridana Le Conte (Coleoptera: Meloidae). VII. Eighty-eight to 132 h: the appendages, the cephalic apodemes, and head segmentation. Can J Zool 49:1571–1581

    Google Scholar 

  • Rousset A (1966) Morphologie cephalique des larves de Planipennes (Insectes — Nevropteroides). Mem Mus Nat Hist Nat Paris (A, Zool) 42:1–199

    Google Scholar 

  • Schoeller J (1964) Recherches descriptives et experimentales sur la cephalogenese de Calliphora erythrocephala (Meigen), au cours des developpements embryonnaire et postembryonnaire. Arch Zool Exp Gen 103:1–216

    Google Scholar 

  • Schoeller-Raccaud J (1977a) Le squelette cephalo-pharyngien de Drosophila melanogaster Meigen, au premier stade larvaire. Bull Soc Ent France 82(3–4):57–62

    Google Scholar 

  • Schoeller-Raccaud J (1977b) La cephalogenese larvaire des Dipteres. In: Grasse P-P (ed) Traite de Zoologie, vol VIII/V-B, pp 262–279. Masson, Paris, New York, Barcelona, Milano

    Google Scholar 

  • Seidel F (1935) Der Anlagenplan im Libellenei, zugleich eine Untersuchung über die allgemeinen Bedingungen für defekte Entwicklung und Regulation bei dotterreichen Eiern. Wilhelm Roux' Arch 132:671–751

    Google Scholar 

  • Singh RN, Singh K (1984) Fine structure of the sensory organs of Drosophila melanogaster Meigen larva (Diptera: Drosophilidae). Int J Insect Morphol Embryol 13:255–273

    Google Scholar 

  • Strasburger M (1932) Bau, Funktion und Variabilität des Darmtractus von Drosophila melanogaster Meigen. Z Wiss Zool 140:539–649

    Google Scholar 

  • Struhl G (1981) A blastoderm fate map of compartments and segments of the Drosophila head. Dev Biol 84:386–396

    Google Scholar 

  • Technau GM, Campos-Ortega JA (1985) Fate-mapping in wild-type Drosophila melanogaster. II. Injections of horseradish peroxidase in cells of the early gastrula stage. Wilhelm Roux's Arch 194:196–212

    Google Scholar 

  • Turner FR, Mahowald AP (1979) Scanning electron microscopy of Drosophila melanogaster embryogenesis. III. Formation of the head and caudal segments. Dev Biol 68:96–109

    Google Scholar 

  • Ullman SL (1964) The origin and structure of the mesoderm and the formation of the coelomic sacs in Tenebrio molitor L. (Insecta, Coleoptera). Phil Trans R Soc (Lond) B 248:245–277

    Google Scholar 

  • Ullmann SL (1967) The development of the nervous system and other ectodermal derivatives in Tenebrio molitor. L. (Insecta, Coleoptera). Phil Trans R Soc Lond B 252:1–25

    Google Scholar 

  • Underwood EM, Turner FR, Mahowald AP (1980) Analysis of cell movements and fate mapping during early embryogenesis in Drosophila melanogaster. Dev Biol 74:286–301

    Google Scholar 

  • Van der Meer J (1977) Optical clean and permanent whole mount preparations for phase contrast microscopy of cuticular structures of insect larvae. Dros Inf Serv 52:160

    Google Scholar 

  • Wada S (1966) Topographie der Anlagenkomplexe der Cephalregion von Tachycines (Saltatoria) beim Keimstreif. Naturwissenschaften 43:414

    Google Scholar 

  • Wundt H (1961) Der Kopf der Larve von Osmylus chryops L. (Neuroptera, Planipennia). Zool J Anat 79:557–662

    Google Scholar 

  • Zacharuk RY, Yin LR, Blue SG (1971) Fine structure of the antenna and its sensory cone in larvae of Aedes aegypti (L.). J Morphol 135:273–298

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jürgens, G., Lehmann, R., Schardin, M. et al. Segmental organisation of the head in the embryo of Drosophila melanogaster . Roux's Arch Dev Biol 195, 359–377 (1986). https://doi.org/10.1007/BF00402870

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00402870

Key words

Navigation