The development of shape. Modular control of growth in the lepidopteran forewing

J Exp Zool B Mol Dev Evol. 2022 May;338(3):170-180. doi: 10.1002/jez.b.23101. Epub 2021 Oct 28.

Abstract

The mechanisms by which tissues and organs achieve their final size and shape during development are largely unknown. Although we have learned much about the mechanisms that control growth, little is known about how those play out to achieve a structure's specific final size and shape. The wings of insects are attractive systems for the study of the control of morphogenesis, because they are perfectly flat and two-dimensional, composed of two closely appressed cellular monolayers in which morphogenetic processes can be easily visualized. The wings of Lepidoptera arise from imaginal disks whose structure is always perfectly congruent with that of the adult wing, so that it is possible to fate-map corresponding positions on the larval disk to those of the adult wing. Here we show that the forewing imaginal disks of Junonia coenia are subdivided into four domains, with characteristic patterns of expression of known patterning genes Spalt (Sal), Engrailed (En), and Cubitus interruptus (Ci). We show that DNA and protein synthesis, as well as mitoses, are spatially patterned in a domain-specific way. Knockdown of Sal and En using produced domain-specific reductions in the shape of the forewing. Knockdown of signaling pathways involved in the regulation of growth likewise altered the shape of the forewing in a domain-specific way. Our results reveal a multi-level regulation of forewing shape involving hormones and growth-regulating genes.

Keywords: engrailed; growth; imaginal disk; morphogenesis; morpholino; spalt.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Butterflies*
  • Larva
  • Morphogenesis / genetics
  • Wings, Animal*