Roux's archives of developmental biology

, Volume 195, Issue 3, pp 145–157 | Cite as

Extra tarsal joints and abnormal cuticular polarities in various mutants ofDrosophila melanogaster

  • Lewis Irving HeldJr.
  • Christine Marie Duarte
  • Kourosh Derakhshanian


The legs of flies from 16 different mutant strains ofDrosophila melanogaster were examined for abnormal cuticular polarities and extra joints. The strains were chosen for study because they manifest abnormal cuticular polarities in some parts of the body (10 strains) or because they have missing or defective tarsal joints (6 strains). All but three of the stocks were found to exhibit misorientations of either the bristles, hairs, or “bract-socket vectors” on the legs. The latter term denotes an imaginary vector pointing from a hairlike structure called a “bract” to the bristle socket with which it is associated. On the legs of wild-type flies nearly all such vectors point distally, as do the bristles and hairs. In the mutant flies, the most common vector misorientation is a 180° reversal. When the bract-socket vectors of adjacent bristle sites in the same bristle row point toward one another, the distance between the sites is frequently abnormally large, whereas when the vectors point in opposite directions, the interval is frequently abnormally small. This correlation is interpreted to mean that bristle cells actively repel one another via cytoplasmic extensions that are longer in the direction of the bract-socket vector than in the opposite direction. Repulsive forces of this kind may be responsible for “fine-tuning” the regularity of bristle spacing in wild-type flies.

Extra tarsal joints were found in eight of the 16 strains. A ninth strain completely lacking tarsal joints appears in some cases to have an extra tibia-basitarsus joint in its tibia. Whereas the tarsi of wild-type flies contain four joints, the tarsi ofspiny legs mutant flies contain as many as eight joints. In this extreme extra-joint phenotype, four of the joints correspond to the normal wild-type joints, and there is an extra joint in every tarsal segment except the distal-most (fifth) segment. Nearly all such ectopic extra joints have inverted polarity. In other strains the extra tarsal joints are located mainly at the wild-type joint sites, and joints of this sort have wild-type polarity. The alternation of normal and inverted (extra) joints inspiny legs resembles the alternation of normal and inverted (extra) body segment boundaries in the embryonic-lethal mutantpatch, suggesting that tarsal and body segmentation may share a common patterning mechanism.

Key words

Drosophila Cell polarity Limb development Pattern formation Bristle 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Albrecht-Buchler G (1977) Daughter 3T3 cells: Are they mirror images of each other? J Cell Biol 72:595–603CrossRefGoogle Scholar
  2. Bohn H (1970) Interkalare Regeneration und segmentale Gradienten bei den Extremitäten vonLeucophaea-Larven (Blattaria). I. Femur und Tibia. Wilhelm Roux's Arch 165:303–341CrossRefGoogle Scholar
  3. Bryant PJ, Schneiderman HA (1969) Cell lineage, growth, and determination in the imaginal leg discs ofDrosophila melanogaster. Dev Biol 20:263–290PubMedCrossRefGoogle Scholar
  4. Bryant PJ, Girton JR, Martin P (1980) Physical and pattern continuity in the insect epidermis. In: Locke M, Smith DS (eds) Insect biology in the future. Academic Press, New York, pp 517–542Google Scholar
  5. Ferris GF (1950) External morphology of the adult. In: Demerec M (ed) Biology ofDrosophila. Hafner Pub Co, New York, pp 368–419Google Scholar
  6. French V, Bryant PJ, Bryant SV (1976) Pattern regulation in epimorphic fields. Science 193:969–981PubMedGoogle Scholar
  7. Garcia-Bellido A, Merriam JR (1971) Clonal parameters of tergite development inDrosophila. Dev Biol 26:264–276PubMedCrossRefGoogle Scholar
  8. Girton JR, Russell MA (1981) An analysis of compartmentalization in pattern duplications induced by a cell-lethal mutation inDrosophila. Dev Biol 85:55–64PubMedCrossRefGoogle Scholar
  9. Gubb D, Garcia-Bellido A (1982) A genetic analysis of the determination of cuticular polarity during development inDrosophila melanogaster. J Embryol Exp Morphol 68:37–57PubMedGoogle Scholar
  10. Hannah-Alava A (1958) Morphology and chaetotaxy of the legs ofDrosophila melanogaster. J Morphol 103:281–310CrossRefGoogle Scholar
  11. Held LI Jr, Pham TT (1983) Accuracy of bristle placement on a leg segment inDrosophila melanogaster. J Morphol 178:105–110CrossRefGoogle Scholar
  12. Hollingsworth MJ (1964) Sex-combs of intersexes and the arrangement of the chaetae on the legs ofDrosophila. J Morphol 115:35–51CrossRefGoogle Scholar
  13. Lawrence PA (1966) Development and determination of hairs and bristles in the milkweed bug,Oncopeltus fasciatus (Lygaeidae, Hemiptera). J Cell Sci 1:475–498PubMedGoogle Scholar
  14. Lawrence PA (1973) The development of spatial patterns in the integument of insects. In: Counce SJ, Waddington CH (eds) Developmental systems: insects, vol 2. Academic Press, New York, pp 157–209Google Scholar
  15. Lee L-W, Gerhart JC (1973) Dependence of transdetermination frequency on the developmental stage of cultured imaginal discs ofDrosophila melanogaster. Dev Biol 35:62–82PubMedCrossRefGoogle Scholar
  16. Lees AD, Waddington CH (1942) The development of the bristles in normal and some mutant types ofDrosophila melanogaster. Proc Roy Soc [Lond] Ser B 131:87–110CrossRefGoogle Scholar
  17. Lindsley DL, Grell EH (1968) Genetic Variations ofDrosophila melanogaster. Carnegie Inst of Washington Publication No 627, Washington DCGoogle Scholar
  18. Locke M, Huie P (1981) Epidermal feet in pupal segment morphogenesis. Tiss Cell 13:787–803Google Scholar
  19. Milner MJ, Bleasby AJ, Pyott A (1983) The role of the peripodial membrane in the morphogenesis of the eye-antennal disc ofDrosophila melanogaster. Wilhelm Roux's Arch 192:164–170CrossRefGoogle Scholar
  20. Nardi JB, Kafatos FC (1976a) Polarity and gradients in lepidopteran wing epidermis. I. Changes in graft polarity, form, and cell density accompanying transpositions and reorientations. J Embryol Exp Morphol 36:469–487PubMedGoogle Scholar
  21. Nardi JB, Kafatos FC (1976b) Polarity and gradients in lepidopteran wing epidermis. II. The differential adhesiveness model: gradient of a non-diffusible cell surface parameter. J Embryol Exp Morphol 36:489–512PubMedGoogle Scholar
  22. Nübler-Jung K (1979) Pattern stability in the insect segment. II. The intersegmental region. Wilhelm Roux's Arch 186:211–233CrossRefGoogle Scholar
  23. Nübler-Jung K (1977) Pattern stability in the insect segment. I. Pattern reconstruction by intercalary regeneration and cell sorting inDysdercus intermedius Dist. Wilhelm Roux's Arch 183:17–40CrossRefGoogle Scholar
  24. Nüsslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity inDrosophila. Nature 287:795–801PubMedCrossRefGoogle Scholar
  25. Poodry CA, Schneiderman HA (1976) Pattern formation melanogaster: The effects of mutations on polarity in the developing leg. Wilhelm Roux's Arch 180:175–188CrossRefGoogle Scholar
  26. Reed CT, Murphy C, Fristrom D (1975) The ultrastructure of the differentiating pupal leg ofDrosophila melanogaster. Wilhelm Roux's Arch 178:285–302CrossRefGoogle Scholar
  27. Russell MA (1985) Positional information in insect segments. Dev Biol 108:269–283CrossRefGoogle Scholar
  28. Russell MA, Girton JR, Morgan K (1977) Pattern formation in a ts-cell-lethal mutant ofDrosophila: the range of phenotypes induced by larval heat treatments. Wilhelm Roux's Arch 183:41–59CrossRefGoogle Scholar
  29. Shaw VK, Bryant PJ (1975) Intercalary leg regeneration in the large milkweed bugOncopeltus fasciatus. Dev Biol 45: 187–191PubMedCrossRefGoogle Scholar
  30. Solomon F (1979) Detailed neurite morphologies of sister neuroblastoma cells are related. Cell 16:165–169PubMedCrossRefGoogle Scholar
  31. Stern C (1954) Genes and developmental patterns.Caryologia. [Suppl] 6:355–369Google Scholar
  32. Tobler H (1969) Beeinflussung der Borstendifferenzierung und Musterbildung durch Mitomycin beiDrosophila melanogaster. Experientia 25:213–214PubMedCrossRefGoogle Scholar
  33. Tobler H, Maier V (1970) Effect of nitrogen mustard on the development of the bristle organ and on the rate of transdetermination ofDrosophila melanogaster. Wilhelm Roux's Arch 164:303–312CrossRefGoogle Scholar
  34. Tobler H, Rothenbühler V, Nöthiger R (1973) A study of the differentiation of bracts inDrosophila melanogaster using two mutations,H 2 andsv de. Experientia 29: 370–371PubMedCrossRefGoogle Scholar
  35. Tokunaga C, Stern C (1969) Determination of bristle direction inDrosophila. Dev Biol 20: 411–425PubMedCrossRefGoogle Scholar
  36. Tokunaga C, Gerhart JC (1976) The effect of growth and joint formation on bristle pattern inD. melanogaster. J Exp Zool 198: 79–96PubMedCrossRefGoogle Scholar
  37. Toney JV, Thompson JN, Jr (1980) Developmental control of the orientation of cuticular structures inDrosophila. Experientia 36: 644–645CrossRefGoogle Scholar
  38. Waddington CH (1940) Genes as evocators in development. Growth [Suppl] 37–44Google Scholar
  39. Walt H, Tobler H (1978) Ultrastructural analysis of differentiating bristle organs in wild-type,shaven-depilate, and Mitomycin C-treated larvae ofDrosophila melanogaster. Biol Cell 32: 291–298Google Scholar
  40. Wright DA, Lawrence PA, (1981) Regeneration of the segment boundary inOncopeltus. Dev Biol 85:317–327PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1986

Authors and Affiliations

  • Lewis Irving HeldJr.
    • 1
  • Christine Marie Duarte
    • 1
  • Kourosh Derakhshanian
    • 1
  1. 1.Developmental Biology CenterUniversity of CaliforniaIrvineUSA

Personalised recommendations