Paleozoic Nymphal Wing Pads Support Dual Model of Insect Wing Origins

Abstract

The appearance of wings in insects, early in their evolution [1], has been one of the more critical innovations contributing to their extraordinary diversity. Despite the conspicuousness and importance of wings, the origin of these structures has been difficult to resolve and represented one of the "abominable mysteries" in evolutionary biology [2]. More than a century of debate has boiled the matter down to two competing alternatives-one of wings representing an extension of the thoracic notum, the other stating that they are appendicular derivations from the lateral body wall. Recently, a dual model has been supported by genomic and developmental data [3-6], representing an amalgamation of elements from both the notal and pleural hypotheses. Here, we reveal crucial information from the wing pad joints of Carboniferous palaeodictyopteran insect nymphs using classical and high-tech techniques. These nymphs had three pairs of wing pads that were medially articulated to the thorax but also broadly contiguous with the notum anteriorly and posteriorly (details unobservable in modern insects), supporting their overall origin from the thoracic notum as well as the expected medial, pleural series of axillary sclerites. Our study provides support for the formation of the insect wing from the thoracic notum as well as the already known pleural elements of the arthropodan leg. These results support the unique, dual model for insect wing origins and the convergent reduction of notal fusion in more derived clades, presumably due to wing rotation during development, and they help to bring resolution to this long-standing debate.

Wing Tracheation in Chrysopidae and Other Neuropterida (Insecta): A Resolution of the Confusion about Vein Fusion

“…By adopting the use of tracheation, we do not imply anything regarding wing origins as it relates to the defunct "exite" or "gill hypothesis" for overall wing homology, that is, wings as serial homologs with abdominal gills found in some crown-group naiads (e.g., Landois, 1871;Wigglesworth, 1976;Kukalová-Peck, 1978, 1983, 1991, which is in opposition to the "paranotal hypothesis" (e.g., Müller, 1873aMüller, , 1873bMüller, , 1875Crampton, 1916;Hamilton, 1971Hamilton, , 1972aWootton, 1976;Rasnitsyn, 1981). Instead, wings have been more recently determined to be of largely notal origin with the incorporation of subcoxal elements to form an articulation at the base, also known as the dual model hypothesis (e.g., Grimaldi and Engel, 2005;Niwa et al, 2010;Engel et al, 2013;Prokop et al, 2017). In this context, the tracheae of the wing represent nothing more than similar tracheation of any body structure.…”

“…In fact, no extinct or extant taxa are documented in which there are paired stems at each axillary point (i.e., paired stems at the base for each longitudinal vein system). Moreover, recent evidence from the nymphal pads of Palaeodictyoptera (Prokop et al, 2017) tends to support Hamilton's (1972a) hypothesis regarding the groundplan venation for insect wings, one that does not include paired, basal stems.…”

“…The wing venation of insects has been a matter of contention and controversy for well over a century (e.g., Hagen, 1870;Adolf, 1879;Brauer, 1885;Redtenbacher, 1886;Brauer and Redtenbacher, 1888;Comstock, 1918;Lameere, 1922Lameere, , 1923Martynov, 1924Martynov, , 1930Needham, 1935;Hamilton, 1972a), and while many fundamental elements have been established an equal or greater number of details remain fiercely debated (e.g., Nel, 2001, 2002;Kukalová-Peck and Lawrence, 2004;Rasnitsyn, 2007;Béthoux, 2008;Engel et al, 2013;Prokop et al, 2017). In more recent history, confusion over vein homologies, combined with perceptions of either putative lability or overconservatism within a given lineage, has led some researchers to discount the systematic value of wings in favor of genitalic structures.…”

What serial homologs can tell us about the origin of insect wings

“…While we were revising this manuscript, Prokop et al reported very intriguing findings that provide support for a dual origin of insect wings from the paleoentomological point of view 59 . Collaboration among various fields, including paleontology and evo-devo, will be fruitful to tackle this century-old question regarding the evolutionary origin of insect wings.…”

Research on Biomimetic Models and Nanomechanical Behaviour of Membranous Wings of Chinese Bee Apis cerana cerana Fabricius

“…The model design imitating insect membranous wings has practical significance. The insect species is more and the forms of membranous wings are complicated and varied, which provides abundant natural sources for the research on biomimetic thin-film materials and biomimetic 2-dimensional composite materials [8, 9]. There are many factors affecting the model imitating insect membranous wings, such as the material property of veins and membranes, distribution and quantity of veins, and appearance of membranous wings [10–12].…”