A new A-P compartment boundary and organizer in holometabolous insect wings

Roohollah Abbasi,Jeffrey M Marcus

doi:10.1038/s41598-017-16553-5

Abstract

Decades of research on the highly modified wings of Drosophila melanogaster has suggested that insect wings are divided into two Anterior-Posterior (A-P) compartments separated by an axis of symmetry. This axis of symmetry is created by a developmental organizer that establishes symmetrical patterns of gene expression that in turn pattern the A-P axis of the wing. Butterflies possess more typical insect wings and butterfly wing colour patterns provide many landmarks for studies of wing structure and development. Using eyespot colour pattern variation in Vanessa butterflies, here we show an additional A-P axis of symmetry running between wing sectors 3 and 4. Boundaries of Drosophila mitotic clones suggest the existence of a previously undetected Far-Posterior (F-P) compartment boundary that coincides with this additional A-P axis. A similar compartment boundary is evident in butterfly mosaic gynandromorphs. We suggest that this additional compartment boundary and its associated developmental organizer create an axis of wing colour pattern symmetry and a gene expression-based combinatorial code, permitting each insect wing compartment to acquire a unique identity and allowing for the individuation of butterfly eyespots.

Highlights

The anterior-posterior (A-P) axis of Drosophila melanogaster wings is typically divided into two developmental wing compartments that were first discovered by genetic mosaic analysis using mitotic clones[1]
We addressed this question by examining the eyespot morphology of 22 Vanessa butterfly species, a genus known for highly diverse eyespot phenotypes[6], and determining whether these proposed
We hypothesized the existence of an additional compartment boundary and a developmental organizer in the posterior portion of the wing that may be responsible for the symmetrical eyespot associations found in Vanessa in this study and in other species by previous authors[12,13,14,15]

Summary

Introduction

The anterior-posterior (A-P) axis of Drosophila melanogaster wings is typically divided into two developmental wing compartments that were first discovered by genetic mosaic analysis using mitotic clones[1]. We re-examined these eyespot associations by asking whether genetically associated eyespots individuate in similar ways We addressed this question by examining the eyespot morphology of 22 Vanessa butterfly species, a genus known for highly diverse eyespot phenotypes[6], and determining whether these proposed www.nature.com/scientificreports/. In Drosophila wings, the A-P wing compartment boundary has an associated developmental organizer that produces symmetrical gene expression domains on either side of the boundary[17]. We hypothesized the existence of an additional compartment boundary and a developmental organizer in the posterior portion of the wing that may be responsible for the symmetrical eyespot associations found in Vanessa in this study and in other species by previous authors[12,13,14,15]. We propose a developmental model for eyespot individuation and insect wing A-P patterning

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Conclusion