Out from under the wing: reconceptualizing the insect wing gene regulatory network as a versatile, general module for body-wall lobes in arthropods

Abstract

Body plan evolution often occurs through the differentiation of serially homologous body parts, particularly in the evolution of arthropod body plans. Recently, homeotic transformations resulting from experimental manipulation of gene expression, along with comparative data on the expression and function of genes in the wing regulatory network, have provided a new perspective on an old question in insect evolution: how did the insect wing evolve? We investigated the metamorphic roles of a suite of 10 wing- and body-wall-related genes in a hemimetabolous insect, Oncopeltus fasciatus . Our results indicate that genes involved in wing development in O. fasciatus play similar roles in the development of adult body-wall flattened cuticular evaginations. We found extensive functional similarity between the development of wings and other bilayered evaginations of the body wall. Overall, our results support the existence of a versatile development module for building bilayered cuticular epithelial structures that pre-dates the evolutionary origin of wings. We explore the consequences of reconceptualizing the canonical wing-patterning network as a bilayered body-wall patterning network, including consequences for long-standing debates about wing homology, the origin of wings and the origin of novel bilayered body-wall structures. We conclude by presenting three testable predictions that result from this reconceptualization.

The hierarchical basis of serial homology and evolutionary novelty

“…It is possible that helmets are serially homologous to wings because they belong to an exite‐derived character family, or the character family of some other basal character, without helmets being wings . Indeed, this seems to be the case (DiFrisco, Wagner & Love, 2022; Fisher et al, 2021). Thus, despite the name “wing serial homologs,” which is commonly used to describe research in this area, wings are evidently too derived to serve as the most evolutionarily informative character for defining the character tree of pleural and tergal outgrowths.…”

“…Similarly, a recent dual-origin theory holds that wings and other body wall outgrowths are derived products of an ancestral developmental network that regulates three-dimensional patterning of cuticularized bilayered epithelia (Fisher et al, 2021). In this interpretation, the basal character would be "bilayered epithelial outgrowths" and the associated ChIM would be the ancestral regulatory network that patterns all such structures.…”

“…character, without helmets being wings. Indeed, this seems to be the case Fisher et al, 2021). Thus, despite the name "wing serial homologs," which is commonly used to describe research in this area, wings are evidently too derived to serve as the most evolutionarily informative character for defining the character tree of pleural and tergal outgrowths.…”

The roles of growth regulation and appendage patterning genes in the morphogenesis of treehopper pronota

“…Although genes expressed in wings are also expressed in the pronotum, a more nuanced interpretation of the significance of this association is required [ 55 , 56 ]. We suggest that two things must be considered when investigating questions related to treehopper pronotal development and evolution: (i) the genes frequently studied in wings, such as wingless, distal-less, engrailed, hedgehog, spalt, decapentaplegic, apterous, vestigial , are also expressed in, and responsible for the patterning of, other appendages including legs, antennae, mouthparts and genitalia, and also play critical roles earlier, in embryonic development [ 2 , 21 , 57 , 58 ]; and (ii) our observations show that many general features of the adult pronotum are already evident in the 4th instar ( figure 3 ), which suggests that critical transcriptional patterning of pronotal differentiation occurs before the 5th instar.…”

Ghost Hunting: Insects Retain Ancestral Abdominal Legs in a Truncated Form

“…Insect tracheae may be internalized crustacean gills (Fig. 4) 34 ; insect wings, tergal plates, helmets, horns, and other ectodermal outgrowths likely evolved from crustacean plate-type outgrowths 3,5,52 ; and insect secretory glands (salivary, endocrine, exocrine, etc) may have evolved from similar glands in crustaceans 40,53,54 . Surprisingly, respiratory organs and secretory glands can be homeotically transformed into each other 40,53,54 and plate-type outgrowths arise from the same tissue as respiratory organs 55 , therefore all three types of structures may have arisen from a common embryonic exite-like structure on the lateral side of the proximal 8 th leg segment [3][4][5] that was inherited from the ancestor of all arthropods.…”