A wing growth organizer in a hemimetabolous insect suggests wing origin

Abstract

The origin and evolution of insect wings remain enigmatic after a century-long discussion. Molecular dissection of wing development in hemimetabolous insects, in which the first functional wings evolved, is key to understand genetic changes required for wing evolution. We investigated Drosophila wing marker genes in the cricket, Gryllus bimaculatus, and found apterous and vestigial show critical functions in nymphal tergal identity and margin formation, respectively. We further demonstrate that margin cells in the lateral-anterior tergal region constitute a growth organizer of wing blades. Transcriptome and RNAi analyses unveiled that Wnt, Fat-Dachsous, and Hippo pathways are involved in disproportional growth of Gryllus wings. Our data collectively support the idea that tergal margin cells of a wingless ancestor gave rise to the body wall extension required for evolution of the first powered flight.