title: Origin and diversification of wings: Insights from a neopteran insect.
abstract: Winged insects underwent an unparalleled evolutionary radiation, but mechanisms underlying the origin and diversification of wings in basal insects are sparsely known compared with more derived holometabolous insects. In the neopteran species Oncopeltus fasciatus, we manipulated wing specification genes and used RNA-seq to obtain both functional and genomic perspectives. Combined with previous studies, our results suggest the following key steps in wing origin and diversification. First, a set of dorsally derived outgrowths evolved along a number of body segments including the first thoracic segment (T1). Homeotic genes were subsequently co-opted to suppress growth of some dorsal flaps in the thorax and abdomen. In T1 this suppression was accomplished by Sex combs reduced, that when experimentally removed, results in an ectopic T1 flap similar to prothoracic winglets present in fossil hemipteroids and other early insects. Global gene-expression differences in ectopic T1 vs. T2/T3 wings suggest that the transition from flaps to wings required ventrally originating cells, homologous with those in ancestral arthropod gill flaps/epipods, to migrate dorsally and fuse with the dorsal flap tissue thereby bringing new functional gene networks; these presumably enabled the T2/T3 wing's increased size and functionality. Third, "fused" wings became both the wing blade and surrounding regions of the dorsal thorax cuticle, providing tissue for subsequent modifications including wing folding and the fit of folded wings. Finally, Ultrabithorax was co-opted to uncouple the morphology of T2 and T3 wings and to act as a general modifier of hindwings, which in turn governed the subsequent diversification of lineage-specific wing forms.
authors.affiliation: Department of Biological Sciences, Wayne State University, Detroit, MI 48202;
authors.forename: Victor
authors.initials: V
authors.lastname: Medved
authors.affiliation: Department of Biology, Pennsylvania State University, University Park, PA 16802; Huck Institutes for the Life Sciences, Pennsylvania State University, University Park, PA 16802;
authors.forename: James H
authors.initials: JH
authors.lastname: Marden
authors.affiliation: Department of Biology, Pennsylvania State University, University Park, PA 16802;
authors.forename: Howard W
authors.initials: HW
authors.lastname: Fescemyer
authors.affiliation: Department of Biology, Pennsylvania State University, University Park, PA 16802; Department of Biological Sciences, California State University, Fullerton, CA 92834.
authors.forename: Joshua P
authors.initials: JP
authors.lastname: Der
authors.affiliation: Department of Biological Sciences, Wayne State University, Detroit, MI 48202;
authors.forename: Jin
authors.initials: J
authors.lastname: Liu
authors.affiliation: Department of Biological Sciences, Wayne State University, Detroit, MI 48202;
authors.forename: Najmus
authors.initials: N
authors.lastname: Mahfooz
authors.affiliation: Department of Biological Sciences, Wayne State University, Detroit, MI 48202; apopadic@biology.biosci.wayne.edu.
authors.forename: Aleksandar
authors.initials: A
authors.lastname: Popadić
mesh_terms: D000818:Animals; D019143:Evolution, Molecular; D018507:Gene Expression Regulation, Developmental; D014644:Genetic Variation; D049750:Genome, Insect / Q000235:genetics; D059014:High-Throughput Nucleotide Sequencing / Q000379:methods; D019476:Insect Proteins / Q000235:genetics; D007313:Insecta / Q000033:anatomy & histology / Q000235:genetics* / Q000254:growth & development; D034622:RNA Interference; D020133:Reverse Transcriptase Polymerase Chain Reaction; D014921:Wings, Animal / Q000033:anatomy & histology / Q000254:growth & development / Q000378:metabolism*
chemical_list: D019476:Insect Proteins
keywords: RNA-seq; Sex combs reduced; Ultrabithorax; vestigial; wing origins