Skip to main content

Histological analysis of the dynamics of growth of imaginal discs and histoblast nests during the larval development ofDrosophila melanogaster

Summary

  1. 1.

    Histological analyses were made of imaginal discs and histoblasts during the larval development ofDrosophila melanogaster to determine the number of cells, the patterns of cell division and the growth dynamics in these adult primordia. Histological studies were also made of the imaginal rings which are the primordia of the adult salivary gland, fore-and hindgut, the anlage cells of the midgut and several larval and embryonic tissues.

  2. 2.

    In the newly-hatched larva, the immature eye-antenna, wing, haltere, leg and genital discs contain about 70, 38, 20, 36–45 and 64 cells respectively. These numbers include cells destined to form cuticular elements as well as peripodial, tracheal and nerve cells and probably the progenitors of adepithelial cells. The number of cells counted in the various imaginal disc anlagen is 1.5 to 4 times higher than the numbers deduced from genetic mosaic analyses by other investigators and reasons for these differences are given.

  3. 3.

    About 12 h after fertilization, mitosis ceases in all tissues of the embryo except the nervous system. After the larva hatches, mitosis resumes in most of the imaginal anlagen and in some larval tissues. The time of resumption of mitosis in the imaginal anlagen was determined after treating the larvae with colchicine for 2 h.

  4. 4.

    Among the imaginal discs, the eye disc is the first to begin cell division, at about 13–15 h after the hatching of the larva (first instar) followed by the wing (15–17 h), the haltere (18–20 h), the antenna, leg, and genitalia (24–26 h, early second instar), and finally the labial and dorsal prothoracic discs (52–54 h, early third instar). The cell doubling time for various discs was calculated from cell counts and the times agree closely with the doubling times deduced from clonal analyses by other workers: e.g., 7.5 h for the cells of the wing disc.

  5. 5.

    The imaginal ring of the hindgut first shows cell division early in the second instar. The imaginal rings of the foregut and salivary glands, the anlage cells of the midgut and the cells of the segmental lateral tracheal branches begin to divide early in the third instar.

  6. 6.

    The histoblasts which are the anlagen of the integument of the adult abdomen do not increase in number from the time of larval hatching until about 5 h after pupation when they begin to divide. Their behaviour contrasts with that of the histoblasts of the other dipterans such asCalliphora, Musca andDacus, which begin to divide during the second instar.

  7. 7.

    The histoblasts are an integral part of the larval abdominal epidermis and, unlike imaginal disc cells, secrete cuticle during larval life. Each hemisegment consists of an anterior dorsal, a posterior dorsal, and a ventral histoblast nest containing about 13, 6 and 12 cells respectively. The 62 histoblasts in each larval segment represent about 7–8% of the total number of cells that form the integument of that segment.

  8. 8.

    The number of cells in a particular type of histoblast nest was constant for both male and female larvae and among the different abdominal segments, except that the anterior dorsal group of the first and the seventh segments contains fewer cells than those of the other segments. Although the male and female adultDrosophila lack the first abdominal sternite and the male lacks the seventh abdominal tergite and sternite, the ventral histoblast nests of the first and the dorsal and ventral nests of the seventh abdominal segments are present in the larval stages as well as in the prepupa and have the same morphology and cell number as similar nests in the rest of the abdominal segments.

  9. 9.

    The cells of the imaginal discs increase in volume about six-fold and their nuclei increase in volume three-fold between the time of hatching and the initiation of mitosis. The histoblasts increase in volume about 60-fold and their nuclei increase in volume about 25-fold between larval hatching and pupariation.

  10. 10.

    Prior to each cell division, the nuclei of the columnar cells of the disc epithelium and of the histoblasts appear to migrate toward the apical surface of the epithelium. The cells round up and shift toward the apical region where mitosis occurs. After cytokinesis, the daughter cells move back to deeper positions in the epithelium. Because the nuclei of the non-dividing cells continue to lie deep in the epithelium, this intermitotic migration of nuclei gives these epithelia a pseudostratified appearance.

  11. 11.

    Analyses of the growth of larval cells and of organs confirmed the observations of earlier investigators that cell division occurs only in a few larval tissues, whereas growth in the rest of the larval tissues is by cell enlargement and polyteny. During larval life, cell division was detected only in the central nervous system, gonads, prothoracic glands, lymph glands and haemocytes. Each tissue began mitosis at a characteristic stage in larval life. The larval cells that did not divide, grew enormously, e.g., epidermal cells increased in volume 150-fold and their nuclei increased in volume 80-fold.

  12. 12.

    The adepithelial cells, which give rise to some of the imaginal muscles, were first identified between the thick side of the imaginal dise epithelium and the basement membrane at the beginning of the third larval instar (50–52 h). The origin of these precursors of mesodermal structures was analysed and evidence is presented that the adepithelial cells come from the disc epithelium. The question of the origin of the mesoderm of cyclorrhaphan Diptera is reviewed and it is suggested that the imaginal disc ectoderm may become segregated from the rest of the embryo before gastrulation has occurred, that is before the mesoderm has been established.

This is a preview of subscription content, access via your institution.

References

  1. Anderson, D.T.: The embryology ofDacus tryoni. II. Development of imaginal discs in the embryo. J. Embryol. Exp. Morphol.11, 339–351 (1963a)

    Google Scholar 

  2. Anderson, D.T.: The larval development ofDacus tryoni (Frogg.) (Diptera: Trypetidae). I. Larval instars, imaginal discs and haemocytes. Aust. J. Zool.11, 202–218 (1963b)

    Google Scholar 

  3. Anderson, D.T.: The larval development ofDacus tryoni (Frogg.) (Diptera: Trypetidae). II. Development of imaginal rudiments other than the principal discs. Aust. J. Zool.12, 1–8 (1964)

    Google Scholar 

  4. Anderson, D.T.: The comparative embryology of Diptera. Annu. Rev. Entomol.11, 23–46 (1966)

    Google Scholar 

  5. Anderson, D.T.: The development of hemimetabolous insects. In: Development Systems: Insects (C.H. Waddington and S.J. Counce, eds.), pp. 96–165. New York: Academic Press 1972a

    Google Scholar 

  6. Anderson, D.T.: The development of holometabolous insects. In: Developmental Systems: Insects (C.H. Waddington and S.J. Counce, eds.), pp. 166–242. New York: Academic Press 1972a

    Google Scholar 

  7. Auerbach, C.: The development of the legs, wings, and halteres in wild type and some mutant strains ofDrosophila melanogaster. Trans. Roy. Soc. Edin.57, 787–816 (1936).

    Google Scholar 

  8. Bairati, A. Jr.: Preliminary observations on the ultrastructure of the lymph gland cells ofDrosophila melanogaster. In: Electron Microscopy (S.S. Breese, ed., Vol. 2), pp. 1–13, New York: Academic Press 1962

    Google Scholar 

  9. Bautz, A.M.: Chronologie de la mise en place de l'hypoderme imaginal de l'abdomen deCalliphora erythrocephala Meigen (Insecte, Diptere, Brachycere). Arch. Zool. Exp. Gen.112, 157–178 (1971)

    Google Scholar 

  10. Becker, H.J.: Über Röntgenmosaikflecken und Defektmutationen am Auge vonDrosophila und die Entwicklungsphysiologie des Auges. Z. Indukt. Abstamm. Vererbungsl.88, 333–373 (1957)

    PubMed  Google Scholar 

  11. Bhaskaran, G.: Developmental behaviour of the abdominal histoblasts in the housefly. Nature New Biol.241, 94–96 (1973)

    PubMed  Google Scholar 

  12. Bodenstein, D.: The postembryonic development ofDrosophila. In: Biology ofDrosophila (M. Demerec, ed.), pp. 275–367. New York: Wiley and Sons, Inc. 1950

    Google Scholar 

  13. Bodenstein, D.: Effects of radiomimetic substances on embryonic development, with special reference to nitrogen mustards. J. Cell Comp. Physiol.43, 179–205 (1954)

    Google Scholar 

  14. Bownes, M.: A photographic study of development in the living embryo ofDrosophila melanogaster. J. Embryol. Exp. Morphol.33, 789–801 (1975)

    PubMed  Google Scholar 

  15. Bownes, M.: Larval and adult abdominal defects resulting from microcautery of blastoderm stagedDrosophila embryos. J. Exp. Zool.195, 369–392 (1976)

    PubMed  Google Scholar 

  16. Bryant, P.J.: Cell lineage relationships in the imaginal wing disc ofDrosophila melanogaster. Develop. Biol.22, 389–411 (1970)

    PubMed  Google Scholar 

  17. Bryant, P.J.: Pattern formation in the imaginal wing disc ofDrosophila melanogaster: Fate map, regeneration and duplication. J. Exp. Zool.193, 47–77 (1975)

    Google Scholar 

  18. Bryant, P.J.: Pattern formation in imaginal discs. In: Genetics and Biology ofDrosophila (T.R.F. Wright and M. Ashburner, eds.), New York: Academic Press (in press) 1977

    Google Scholar 

  19. Bryant, P.J., Schneiderman, H.A.: Cell lineage, growth, and determination in the imaginal leg discs ofDrosophila melanogaster. Develop. Biol.20, 263–290 (1969)

    PubMed  Google Scholar 

  20. Chan, L.N., Gehring, W.: Determination of blastoderm cells inDrosophila melanogaster. Proc. Nat. Acad. Sci. U.S.A.68, 2217–2221 (1971)

    Google Scholar 

  21. Chen, T.-Y.: On the development of imaginal buds in normal and mutantDrosophila melanogaster. J. Morphol.47, 135–199 (1929)

    Google Scholar 

  22. Chevais, S.: Determinisme de la taille de l'ocil chez le mutantbar de laDrosophile. Intervention d'une substance diffusible specifique. Bull. Biol. Fr. Belg.78, 71–110 (1944)

    Google Scholar 

  23. Déak, I.I.: Personal communication (1976)

  24. El-Shatoury, H.H.: The structure of the lympth glands ofDrosophila larvae. Wilhelm Roux's Archives147, 489–495 (1955)

    Google Scholar 

  25. El-Shatoury, H.H., Waddington, C.H.: Functions of lymph gland cells during the larval period inDrosophila. J. Embryol. Exp. Morphol.5, 122–133 (1957)

    Google Scholar 

  26. Emmert, W.: Entwicklungsleistungen abdominaler Imaginalscheiben vonCalliphora erythrocephala (Insecta, Diptera). Experimentelle Untersuchungen zur Morphologie des Abdomens. Wilhelm Roux's Archives169, 87–133 (1972)

    Google Scholar 

  27. Ferris, G.F.: External morphology of the adult. In: Biology ofDrosophila (M. Demerec, ed.), pp. 268–418. New York: Wiley and Sons, Inc. 1950

    Google Scholar 

  28. French, V., Bryant, P.J., Bryant, S.V.: Pattern regulation in epimorphic fields. Science193, 969–981 (1976)

    PubMed  Google Scholar 

  29. Fugita, S.: The matrix cell and cytogenesis in the developing nervous system. J. Comp. Neurol.120, 37–42 (1963)

    PubMed  Google Scholar 

  30. Fugita, S.: Application of light and electron microscopic autoradiography to the study of cytogenesis of the forebrain. In: Evolution of the Forebrain (R. Hassler and H. Stephan, eds.), pp. 180–196. New York: Plenum Press 1966

    Google Scholar 

  31. Garcia-Bellido, A., Merriam, J.R.: Cell lineage of the imaginal discs inDrosophila gynandromorphs. J. Exp. Zool.170, 61–76 (1969)

    PubMed  Google Scholar 

  32. Garcia-Bellido, A., Merriam, J.R.: Parameters of the wing imaginal disc development ofDrosophila melanogaster. Develop. Biol.24, 61–87 (1971a)

    PubMed  Google Scholar 

  33. Garcia-Bellido, A., Merriam, J.R.: Clonal parameters of tergite development inDrosophila. Develop. Biol.26, 264–276 (1971b)

    PubMed  Google Scholar 

  34. Gehring, W., Nöthiger, R.: The imaginal discs ofDrosophila. In: Developmental Systems: Insects (S.J. Counce, C.H. Waddington, eds.), Vol. 2 New York: Academic Press 1972

    Google Scholar 

  35. Guerra, M., Postlethwait, J.H., Schneiderman, H.A.: The development of the imaginal abdomen ofDrosophila melanogaster. Develop. Biol.32, 361–372 (1973)

    PubMed  Google Scholar 

  36. Haynie, J.: Intercalary regeneration and pattern formation in imaginal discs ofDrosophila melanogaster. Ph.D. Thesis, Univ. Calif., Irvine (1975)

    Google Scholar 

  37. Haynie, J.L., Bryant, P.J.: Intercalary regeneration in imaginal wing disk ofDrosophila melanogaster. Nature259, 659–662 (1976)

    PubMed  Google Scholar 

  38. Haynie, J.L., Bryant, P.J.: Clonal analysis of cell death and regeneration in irradiated imaginal wing discs ofDrosophila melanogaster. Wilhelm Roux's Archives. In press (1977)

  39. Jones, J.C.: Hemocytopoiesis in insects. In: Regulation of Hematopoiesis (Albert S. Gordon, ed.), Vol. 1, pp. 7–65. New York: Appleton-Century-Crofts 1963

    Google Scholar 

  40. Langman, J., Guerrant, R.L., Freeman, B.G.: Behavior of neuroepithelial cells during closure of the neural tube. J. Comp. Neurol.127, 399–412 (1966)

    PubMed  Google Scholar 

  41. Laugé, G.: Mise en place d'éléments mésodermiques dans le disque génital deDrosophila melanogaster Meig. C.R. Acad. Sci. Paris280, 339–342 (1975)

    Google Scholar 

  42. Laugé, G., Grasse, P.P.: Origine et croissance du disque génital deDrosophila melanogaster Meig. C.R. Acad. Sci. Paris265, 814–817 (1967)

    Google Scholar 

  43. Lawrence, P.: Personal communication (1977)

  44. Makino, S.: A morphological study of the nucleus in various kinds of somatic cells ofDrosophila. Cytologia9, 272–282 (1938)

    Google Scholar 

  45. Newby, W.W.: VII. A study of intersexes produced by a dominant mutation inDrosophila virilis, Blanco stock. Univ. Texas Publ.4228, 113–145 (1942)

    Google Scholar 

  46. Newby, W.W., Thelander, R.P.: Early development of the head in normal and tumorous headD. melanogaster. Drosoph. Inform. Serv.24, 89–90 (1950)

    Google Scholar 

  47. Nöthiger, R.: The larval development of imaginal disks. In: The Biology of Imaginal Discs (H. Ursprung, R. Nöthiger, eds.), pp. 1–34. New York: Springer Verlag 1972

    Google Scholar 

  48. Okada, M., Kleinmann, I.A., Schneiderman, H.A.: ChimericDrosophila adults produced by transplantation of nuclei into specific regions of fertilized eggs. Develop. Biol.39, 286–294 (1974)

    PubMed  Google Scholar 

  49. Pearson, M.J.: Imaginal disks and the abdominal histoblasts ofCalliphora erythrocephala (Diptera). Nature238, 349–351 (1972)

    Google Scholar 

  50. Pearson, M.J.: the relation between larval and adult abnormalities in the abdominal segmentation ofCalliphora erythrocephala (Diptera). J. Embryol. exp. Morphol.32, 533–555 (1974)

    PubMed  Google Scholar 

  51. Perez, C.: Recherches histologiques sur la métamorphose des muscides (Calliphora). Arch. Zool. Exp.4, 1–274 (1910)

    Google Scholar 

  52. Poodry, C.A., Schneiderman, H.A.: The ultrastructure of the developing leg ofDrosophila melanogaster. Wilhelm Roux's Archives166, 1044 (1970)

    Google Scholar 

  53. Postlethwait, J.H., Schneiderman, H.A.: A clonal analysis of development inDrosophila melanogaster: Morphogenesis, determination, and growth in the wild-type antenna. Develop. Biol.24, 477–519 (1971)

    PubMed  Google Scholar 

  54. Postlethwait, J.H., Schneiderman, H.A.: Developmental genetics ofDrosophila imaginal discs. Annu. Rev. Genet.7, 381–433 (1974)

    Google Scholar 

  55. Poulson, D.F.: Histogenesis, organogenesis, and differentiation in the embryo ofDrosophila melanogaster Meigen. In: Biology ofDrosophila (M. Demerec, ed.), pp. 168–270. New York: Hafner 1950

    Google Scholar 

  56. Reed, C.T., Murphy, C., Fristrom, D.: The ultrastructure of the differentiating pupal leg ofDrosophila melanogaster. Wilhelm Roux's Archives178, 285–302 (1975)

    Google Scholar 

  57. Ripoll, P.: The embryonic organization of the imaginal wing disc ofDrosophila melanogaster. Wilhelm Roux's Archives169, 200–215 (1972)

    Google Scholar 

  58. Rizki, N.T.N.: Alterations in the haemocyte population ofDrosophila melanogaster. J. Morphol.100, 437–457 (1957)

    Google Scholar 

  59. Robertson, C.W.: The metamorphosis ofDrosophila melanogaster, including an accurately timed account of the principal morphological changes. J. Morphol.59, 351–399 (1936)

    Google Scholar 

  60. Roseland, C.: Regulation and pattern formation in the abdominal histoblasts ofDrosophila melanogaster andMusca domestica. Ph. D. Thesis, Univ. Calif., Irvine, 1976

    Google Scholar 

  61. Santamaria, P., Garcia-Bellido, A.: Localization and growth pattern of the tergite anlage ofDrosophila. J. Embryol. Exp. Morphol.28, 397–417 (1972)

    PubMed  Google Scholar 

  62. Sauer, F.C.: The interkinetic migration of embryonic epithelial nuclei. J. Morphol.60, 1–11 (1936)

    Google Scholar 

  63. Sauer, F.C.: Some factors in the morphogenesis of vertebrate embryonic epithelium. J. Morphol.61, 563–579 (1937)

    Google Scholar 

  64. Sauer, M.E., Chittenden, A.C.: Deoxyribonucleic acid content of cell nuclei in the neural tube of the chick embryo: evidence for inter-mitotic migration of nuclei. Exp. Cell Res.16, 1–6 (1959)

    PubMed  Google Scholar 

  65. Sauer, M.E., Walker, B.E.: Radioautographic study of interkinetic nuclear migration in the neural tube. Proc. Soc. Exp. Biol. Med.101, 557–560 (1959)

    PubMed  Google Scholar 

  66. Shearn, A., Garen, A.: Genetic control of imaginal disc development inDrosophila. Proc. Nat. Acad. Sci., U.S.A.71, 1393–1397 (1974)

    Google Scholar 

  67. Snodgrass, R.E.: Anatomy and metamorphosis of the apple maggot,Rhagoletic pomonella Walsh. J. Agri. Res.28, 1–36 (1924)

    Google Scholar 

  68. Sonneblick, B.P.: The early embryology ofDrosophila melanogaster. In: Biology ofDrosophila, (M. Demerec, ed.), pp. 62–163. New York: Hafner 1950

    Google Scholar 

  69. Stark, M.B., Marshall, A.K.: The blood-forming organ of the larva ofDrosophila melanogaster. Amer. Inst. Homeopat.23, 1204–1206 (1930)

    Google Scholar 

  70. Trager, W.: The relation of cell size to growth in insect larvae. J. Exp. Zool.71, 489–508 (1935)

    Google Scholar 

  71. Ursprung, H., Conscience-Egli, M., Fox, D.J., Wallimann, T.: Origin of leg musculature duringDrosophila metamorphosis. Proc. Nat. Acad. Sci. U.S.A.69, 2812–2813 (1972)

    Google Scholar 

  72. Whitten, J.M.: Haemocytes and the metamorphosing tissues inSarcophaga bullata, Drosophila melanogaster, and other cyclorrhaphous Diptera. J. Insect Physiol.10, 447–469 (1964)

    Google Scholar 

  73. Wieschaus, E.: Clonal analysis of early development inDrosophila melanogaster. Ph. D. Thesis, Yale University 1975

  74. Wieschaus, E., Gehring, W.: Clonal analysis of primordial disc cells in the early embryo ofDrosophila melanogaster. Develop. Biol.50, 249–263 (1976)

    PubMed  Google Scholar 

  75. Zwaan, J., Bryan, Jr., P.R., Pearson, J.L.: Interkinetic nuclear migration during the early stages of lens formation in the chicken embryo. J. Embryol. Exp. Morphol.21, 71–83 (1969)

    PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Howard A. Schneiderman.

Additional information

We dedicate this paper to the memory of our dear colleague Dr. Elizabeth B. Fosket (1941–1973) who was involved in early phases of this research and was deeply interested in the problems we have analysed

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Mandaravally Madhavan, M., Schneiderman, H.A. Histological analysis of the dynamics of growth of imaginal discs and histoblast nests during the larval development ofDrosophila melanogaster . Wilhelm Roux' Archiv 183, 269–305 (1977). https://doi.org/10.1007/BF00848459

Download citation

Key words

  • Drosophila
  • Imaginal disc
  • Histoblasts
  • Adepithelial cells