Evolutionary origin of the insect wing via integration of two developmental modules

Abstract

Insect wing is a key evolutionary innovation for insect radiation, but its origins and intermediate forms are absent from the fossil record. To understand the ancestral state of the wing, expression of three key regulatory genes in insect wing development, wingless (wg), vestigial (vg), and apterous (ap) was studied in two basal insects, mayfly and bristletail. These basal insects develop dorsal limb branches, tracheal gill and stylus, respectively, that have been considered candidates for wing origin. Here we show that wg and vg are expressed in primordia for tracheal gill and stylus. Those primordia are all located in the lateral body region marked by down-regulation of early segmental wg stripes, but differ in their dorsal-ventral position, indicating their positions drifted within the lateral body region. On the other hand, ap expression was detected in terga of mayfly and bristletail. Notably, the extensive outgrowth of the paranotal lobe of apterygote bristletail developed from the border of ap-expressing tergal margin, and also expressed wg and vg. The data suggest that two regulatory modules involving wg-vg are present in apterygote insects: one associated with lateral body region and induces stick-like dorsal limb branches, the other associated with the boundary of dorsal and lateral body regions and the flat outgrowth of their interface. A combinatorial model is proposed in which dorsal limb branch was incorporated into dorsal-lateral boundary and acquired flat limb morphology through integration of the two wg-vg modules, allowing rapid evolution of the wing.

Origin and diversification of wings: Insights from a neopteran insect

“…Furthermore, nub affected leg-adjacent morphology of the Oncopeltus T1 ventral thorax and was expressed only in the blade portion of the T2 wing but not the adjacent scutellum, similar to the way nub is expressed only in the posterior compartment of crustacean gills (23). Starting with fossil evidence (42) and continuing with developmental data (18,23,25,32,33) and present insights from Oncopeltus, genes expressed in crustacean gills appear to mark a cell population that evolved into both tracheae and wings in insects. In wings, the fusion of both dorsal and ventral contributions appears to be required for formation of fully developed and functional wings.…”

Dpp-induced Egfr signaling triggers postembryonic wing development in Drosophila

“…Dorsal appendages such as the tracheal gill or stylus are like the Drosophila wing in that they express wg and vg and may represent evolutionary precursors to the wing (54). Unlike the wing, however, they do not form close to a region where ap is also expressed, which may be essential for an outgrowth to form a flat structure like the wing (54). Vn/Egfr signaling is upstream of ap and therefore a prerequisite for wing formation (12).…”

“…In a combination of these ideas, it has been proposed that the wing may have a leg origin but that the ability to form a flat wing-like structure depends upon proximity to the dorsal-lateral boundary in the side body (the paranotal lobe in wingless forms) (54). Dorsal appendages such as the tracheal gill or stylus are like the Drosophila wing in that they express wg and vg and may represent evolutionary precursors to the wing (54). Unlike the wing, however, they do not form close to a region where ap is also expressed, which may be essential for an outgrowth to form a flat structure like the wing (54).…”

Wing Tracheation in Chrysopidae and Other Neuropterida (Insecta): A Resolution of the Confusion about Vein Fusion

“…By adopting the use of tracheation, we do not imply anything regarding wing origins as it relates to the defunct "exite" or "gill hypothesis" for overall wing homology, that is, wings as serial homologs with abdominal gills found in some crown-group naiads (e.g., Landois, 1871;Wigglesworth, 1976;Kukalová-Peck, 1978, 1983, 1991, which is in opposition to the "paranotal hypothesis" (e.g., Müller, 1873aMüller, , 1873bMüller, , 1875Crampton, 1916;Hamilton, 1971Hamilton, , 1972aWootton, 1976;Rasnitsyn, 1981). Instead, wings have been more recently determined to be of largely notal origin with the incorporation of subcoxal elements to form an articulation at the base, also known as the dual model hypothesis (e.g., Grimaldi and Engel, 2005;Niwa et al, 2010;Engel et al, 2013;Prokop et al, 2017). In this context, the tracheae of the wing represent nothing more than similar tracheation of any body structure.…”