Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Evidence for Notch-mediated lateral inhibition in organizing butterfly wing scales

Abstract

Here I present gene expression data that implicate a Notch-mediated lateral inhibition process in the spatial organization of butterfly wing scales. During early pupal development the receptor molecule Notch is expressed in a grid-like pattern in the wing epithelium, resulting in parallel rows of uniformly spaced cells with low Notch expression. Previous work has shown that these low-Notch cells express a homolog of the achaete-scute proneural transcription factors and develop into scales. All of these observations are consistent with the Drosophila model of Notch-mediated bristle determination and support the hypothesis that bristles and scales share an underlying patterning mechanism.

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

Fig. 1A–C

References

  1. Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284:770–776

  2. Brunetti CR, Selegue JE, Monteiro A, French V, Brakefield PM, Carroll SB (2001) The generation and diversification of butterfly eyespot color patterns. Curr Biol 11:1578–1585

  3. Calleja M, Renaud O, Usui K, Pistillo D, Morata G, Simpson P (2002) How to pattern an epithelium: lessons from achaete-scute regulation on the notum of Drosophila. Gene 292:1–12

  4. Fehon RG, Kooh PJ, Rebay I, Regan CL, Xu T, Muskavitch MAT, Artavanis-Tsakonas S (1990) Molecular interactions between the protein products of the neurogenic loci Notch and Delta, 2 EGF-homologous genes in Drosophila. Cell 61:523–534

  5. Galant R, Skeath JB, Paddock S, Lewis DL, Carroll SB (1998) Expression pattern of a butterfly achaete-scute homolog reveals the homology of butterfly wing scales and insect sensory bristles. Curr Biol 8:807–813

  6. Honda H, Tanemura M, Yoshida A (2000) Differentiation of wing epidermal scale cells in a butterfly under the lateral inhibition model—appearance of large cells in a polygonal pattern. Acta Biotheoret 48:121–136

  7. Koch PB, Merk R, Reinhardt R, Weber P (2003) Localization of ecdysone receptor protein during colour pattern formation in wings of the butterfly Precis coenia (Lepidoptera: Nymphalidae) and co-expression with Distal-less protein. Dev Genes Evol 212:571–584

  8. Mayer AG (1896) The development of the wing scales and their pigment in butterflies and moths. Bull Mus Comp Zool 29:209–236

  9. Nardi JB, Magee-Adams SM (1986) Formation of scale spacing patterns in a moth wing. 1. Epithelial feet may mediate cell rearrangement. Dev Biol 116:278–290

  10. Nijhout HF (1991) The development and evolution of butterfly wing patterns. Smithsonian Institution Press, Washington, D.C.

  11. Overton J (1966) Microtubules and microfibrils in morphogenesis of the scale cells of Ephestia kühniella. J Cell Biol 29:293–305

  12. Panganiban G, Sebring A, Nagy L, Carroll S (1995) The development of crustacean limbs and the evolution of arthropods. Science 270:1363–1366

  13. Scoble MJ (1992) The Lepidoptera: form, function, and diversity. Oxford University Press, Oxford

  14. Simpson P, Woehl R, Usui K (1999) The development and evolution of bristle patterns in Diptera. Development 126:1349–1364

  15. Wigglesworth V (1972) The principles of insect physiology. Methuen, New York

  16. Yoshida A, Aoki K (1989) Scale arrangement pattern in a lepidopteran wing. 1. Periodic cellular pattern in the pupal wing of Pieris rapae. Dev Growth Differ 31:601–609

Download references

Acknowledgements

I thank Lisa M. Nagy and the referees for comments on the manuscript, Sean B. Carroll for the Distal-less antibody, Developmental Studies Hybridoma Bank for the Notch antibody, and W. Owen McMillan for H. erato. This work was supported by National Science Foundation grant DEB 0209441.

Author information

Correspondence to Robert D. Reed.

Additional information

Edited by M. Akam

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Reed, R.D. Evidence for Notch-mediated lateral inhibition in organizing butterfly wing scales. Dev Genes Evol 214, 43–46 (2004). https://doi.org/10.1007/s00427-003-0366-0

Download citation

Keywords

  • Heliconius
  • Bristle
  • Achaete-scute
  • Evolution
  • Development