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

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

Roohollah Abbasi & Jeffrey M. Marcus

Scientific Reports volume 7, Article number: 16337 (2017)

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.

We studied compartment boundaries in holometabolous insects using Vanessa butterflies and the fruitfly Drosophila melanogaster as model organisms. Independent contrast analysis of Vanessa butterflies revealed significant correlations between eyespots 2 and 5 and between eyespots 3 and 4 on all wing surfaces (Table 1), suggesting the presence of an A-P colour pattern organizer centered on the M3 vein. DrosophilaFLP/FRT wing clones do not cross a compartment boundary posterior to vein L5 (Fig. 2a,b), which is homologous to the M3 vein in butterflies (Fig. 1). A survey of lepidopteran mosaic gynandromorphs and homeotic mosaics with large clones suggests that a similar compartment boundary occurs in a homologous location (Fig. 2c). Collectively, these findings suggest the existence of a Far-Posterior compartment boundary and an associated positional organizer along the M3 vein between wing sectors 3 and 4 in holometabolous insect wings. We propose a model that provides a mechanistic explanation for both consistent phenotypic correlations between eyespots and the diverse evolutionary opportunities for individuation of serially homologous eyespots.

 

A refutation to ‘A new A-P compartment boundary and organizer in holometabolous insect wings.’

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A refutation to ‘A new A-P compartment boundary and organizer in holometabolous insect wings.’

Peter A. Lawrence Jose Casal Jose F. de CelisGines Morata
We respond to a recent report by Abbasi and Marcus who present two main findings:
first they argue that there is an organiser and a compartment boundary within the posterior compartment of the butterfly wing.
Second, they present evidence for a previously undiscovered lineage boundary near wing vein 5 in Drosophila, a boundary that delineates a “far posterior” compartment.
Clones of cells were marked with the yellow mutation and they reported that these clones always fail to cross a line close to vein 5 on the Drosophila wing. In our hands yellow proved an unusable marker for clones in the wing blade and therefore we reexamined the matter.
We marked clones of cells with multiple wing hairs or forked and found a substantial proportion of these clones cross the proposed lineage boundary near vein 5, in conflict with their findings and conclusion.
As internal controls we showed that these same clones respect the other two well established compartment boundaries: the anteroposterior compartment boundary is always respected. The dorsoventral boundary is mostly respected, and is crossed only by clones that are induced early in development, consistent with many reports.
We question the validity of Abbasi and Marcus’ conclusions regarding the butterfly wing but present no new data. Arising from: R. Abbasi and J. M. Marcus Sci. Rep. 7, 16337 (2017); https://doi.org/10.1038/s41598-017-16553-5 .