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 geneexpression 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.wing origins | Sex combs reduced | Ultrabithorax | RNA-seq | vestigial S ome 350 million years ago, the development of insect wings was a seminal event in the evolution of insect body design (1, 2). The ability to fly was critical to insects becoming the most diverse and abundant animal group, and the origin of such novelty has been a focus of intense scientific inquiry for more than a century (3, 4). More recently, through studies of genetic model systems such as Drosophila, the mechanisms of wing morphogenesis have been elucidated (5-12). Still lacking however is a comprehensive understanding of transitional steps connecting the morphology of structures observed in the fossil record with that of the modern-day insects, including wing origins and subsequent diversification.The initial stages of insect wing evolution are missing from the fossil record and it is therefore necessary to use indirect evidence from fossils that postdate the origin and initial radiation of pterygotes (2). Larvae of many of those taxa featured dorsally positioned outgrowths on each of the thoracic and abdominal segments (2, 13), apparently serial homologs (i.e., similar structures likely arising from a common set of developmental mechanisms). Diverse lineages independently lost those dorsal appendages on the abdomen while un...

Tergal and pleural structures contribute to the formation of ectopic prothoracic wings in cockroaches

“…This resemblance of dorsal morphology between T1 of Scr -depleted specimens and T2 has been also observed in P. americana [9], as well as in O. fasciatus , where the formation of an ectopic scutellum (which is typical of T2) in T1 is well apparent [7,8], which suggested to the respective authors that Scr depletion triggered a partial transformation of T1 to T2.…”

“…Similar experiments carried out with the Scr orthologue Cephalothorax in the flour beetle, Tribolium castaneum , elicited the formation of elytra in T1 [5], a phenotype that was also observed when depleting Scr expression by RNA interference (RNAi) [6]. More recently, formation of wing-like tissue in T1 after RNAi of Scr has been reported in the large milkweed bug, Oncopeltus fasciatus [7,8], and the American cockroach, Periplaneta americana [9]. …”

A Pathway Analysis of Melanin Patterning in a Hemimetabolous Insect

“…Injections were performed around the beginning of the last nymphal stage (fifth nymphs). Ubx RNAi was performed following an established protocol (Medved et al, 2015). For ebony RNAi, 20 nymphs (1987).]…”

“…In the butterfly Junonia coenia, the Hox gene Ultrabithorax (Ubx) plays such a role by differential regulation of hindwing and forewing color patterns (Weatherbee et al 1999). Recently, Ubx was shown to also control the identity of hindwing in Oncopeltus (Medved et al 2015), allowing us to test the generality of the selector gene's role in regional regulation. Therefore, on depletion of Ubx, we would expect ebony to be expressed in the developing hindwing, whereas aaNAT should be absent.…”

“…The orthologies of these Oncopeltus genes were confirmed by phylogenetic analysis ( Figure S1 and Figure S2). In the case of Oncopeltus Ubx, a previously described clone was used (Medved et al 2015). …”