Abstract
The origin and evolution of the novel insect wing remain enigmatic after a century-long discussion. The mechanism of wing development in hemimetabolous insects, in which the first functional wings evolved, is key to understand where and how insect wings evolutionarily originate. This study explored the developmental origin and the postembryonic dramatic growth of wings in the cricket Gryllus bimaculatus. We find that the lateral tergal margin, which is homologous between apterygote and pterygote insects, comprises a growth organizer to expand the body wall to form adult wing blades in Gryllus. We also find that Wnt, Fat-Dachsous, and Hippo pathways are involved in the disproportional growth of Gryllus wings. These data provide insights into where and how insect wings originate. Wings evolved from the pre-existing lateral terga of a wingless insect ancestor, and the reactivation or redeployment of Wnt/Fat-Dachsous/Hippo-mediated feed-forward circuit might have expanded the lateral terga.
Highlights
The origin and evolution of the novel insect wing remain enigmatic after a century-long discussion
The significance of this development for successful radiation of this animal group is unarguable, yet the evolutionary history of the wing remains unclear after a century-long debate. Both the location and the morphogenetic process of the origin of the insect wing remain elusive[1]. Regarding the former, the degree of contribution of three elements is under discussion: the pleuron and two subdomains of the tergum, i.e. the lateral and bona fide terga, which are derived from the proximal leg segment and the dorsal body wall in an ancestral crustacean, respectively[1,2,3,4]
Because the first winged insects were obviously hemimetabolous species, a dissection of hemimetabolous wing development at the molecular level would help map the developmental origin of wings in the insect body plan and deduce the changes in development that are responsible for the emergence of wings from a wingless body plan
Summary
The origin and evolution of the novel insect wing remain enigmatic after a century-long discussion. Marginal expression patterns of wg and vg in stage 9 embryos are both localized to the lateral to posterior regions of all thoracic segments, and in the anterior region of prothorax (T1) (Fig. 1d, g, j, k). Consistent with the expression pattern during embryogenesis, vg sgRNA/Cas[9] injected individuals (vg crispants) exhibited a lack of tergal margins in both wingless (T1) and wing-bearing (T2 and T3) segments of first instar nymphs (Fig. 2f–h).
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