A wing growth organizer in a hemimetabolous insect suggests wing origin

<jats:title>ABSTRACT</jats:title><jats:p>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<jats:italic>Drosophila</jats:italic>wing marker genes in the cricket,<jats:italic>Gryllus bimaculatus</jats:italic>, and found<jats:italic>apterous</jats:italic>and<jats:italic>vestigial</jats:italic>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<jats:italic>Gryllus</jats:italic>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.</jats:p>