Which structure of the wingless ancestor of winged insects (Pterygota) gave rise to the wing has been debated for over a century and remains unsettled. A mayfly genome and expression study (Almudi et al., Nature Communications 2020) showed that the abdominal gills of the mayfly Cloeon dipterum share transcriptomic similarity with developing wing pads, a result consistent with both the pleural hypothesis (wings derived from a leg exite homologous to crustacean epipods/gills that was incorporated into the body wall) and the dual hypothesis (a composite of tergal and pleural tissues), but not discriminating between them. Literature through 2025 sharpens rather than resolves the question: crustacean leg-segment knockouts support an exite origin, cricket wing development supports a lateral-tergal origin, and Paleozoic fossils support serial wing precursors with a possible respiratory function. The surviving open core is to identify the ancestral structure(s) from which wings evolved and the relative contributions of the tergum, the incorporated leg exite, and the pleuron to the wing, including whether the mayfly gill–wing-pad transcriptomic similarity reflects structural homology or co-option of a conserved gene-regulatory module.

Background

Winged insects (Pterygota) constitute the largest animal radiation on Earth, and the origin of their wings — the defining structure of the group — has been ranked among the classic 'abominable mysteries' of evolutionary biology. Mayflies (Ephemeroptera), together with dragonflies and damselflies (Odonata), are the earliest-diverging surviving winged lineages; their aquatic juveniles (nymphs) breathe through paired abdominal gills (tracheal gills) and carry their developing wings externally as wing pads, which makes mayflies a strategic group for comparing gills and wings.

Three scenarios dominate the debate. The tergal (or 'paranotal') hypothesis derives wings from lateral expansions of the dorsal thoracic body wall plates (the tergum, or notum). The pleural hypothesis derives wings from an exite — an outer branch or outgrowth at the base of the leg — in particular a proximal exite homologous to the epipods (gill-like flaps) on the legs of crustaceans; in this view the wing is a transformed leg branch that became incorporated into the lateral body wall (the pleuron). The dual hypothesis, revived by paleontological and developmental data, holds that the wing is a composite of tergal and pleural/exite tissues.

Key evidence: Carboniferous nymphal fossils show wing pads articulated medially to the thorax (a pleural trait) yet broadly contiguous with the notum (a tergal trait), supporting a dual model (Prokop et al. 2017). The mayfly Cloeon dipterum genome revealed an expanded repertoire of odorant-binding proteins (OBPs, small secreted proteins that carry hydrophobic odorants to receptors), many expressed specifically in nymphal gills, and a shared set of 126 orthologous gene families expressed in the wing-development modules of mayfly and Drosophila; the gill–wing-pad transcriptomic similarity is consistent with both pleural and dual scenarios but does not distinguish them (Almudi et al. 2020). Knockout of five leg-patterning genes in the crustacean Parhyale hawaiensis led Bruce and Patel (2020) to propose that two ancestral leg segments were incorporated into the insect body wall, carrying a proximal leg exite onto the back to form the wings — an exite (pleural/dual) origin. Wing-related tissues in the German cockroach likewise support a dual origin (Clark-Hachtel et al. 2021). However, studies of wing gene-regulatory networks (GRNs, the sets of interacting regulatory genes that build an organ) show that wing-patterning genes form a versatile module deployed in many non-wing body-wall outgrowths (Fisher et al. 2021), so gene-expression similarity between organs does not by itself establish that the organs share an evolutionary origin (homology) rather than redeployment of the same developmental program (co-option). On the tergal side, work on cricket (Gryllus) wing development identified the lateral tergal margin as the growth organizer that expands into the wing blade (Ohde et al. 2022). Paleozoic fossils with serial lateral outgrowths on thorax and abdomen, some of them gill-like, support an ancestor bearing repeated wing precursors that may have functioned in respiration (Prokop et al. 2022; Prokop et al. 2023). A 2025 review by Ohde and Prokop concludes that recent evo-devo work 'reframes' the debate around a modern exite-incorporation hypothesis, with the current open focus being the relative contributions of the incorporated exite homolog, the pleuron, and the medial tergum to wing evolution. Thus the century-old question of where the wing came from survives, now in the sharpened form of which tissues, in what proportions, built the first wings.

Problem Statement

Determine the evolutionary origin of insect wings: which structure(s) of the wingless (apterygote-grade) ancestor of winged insects gave rise to the wing, and in what relative proportions — (i) lateral outgrowths of the dorsal thoracic body wall (tergum/notum; the tergal or 'paranotal' hypothesis); (ii) a proximal leg exite homologous to crustacean epipods (and, in mayflies, akin to gills) that was incorporated into the insect body wall (the pleural hypothesis); or (iii) a composite of tergal and pleural/exite tissues (the dual hypothesis). A resolving answer must (a) discriminate among these scenarios with evidence that cannot be reinterpreted as compatible with all of them at once, and (b) establish, by developmental origin, the relative contributions of the incorporated exite homolog, the pleuron (the lateral body wall into which it was incorporated), and the tergum to the mature wing of the ancestral pterygote — allowing a pure tergal resolution in which the exite and pleural contributions are zero. It must also adjudicate the specific evidential question raised by the mayfly genome study: whether the transcriptomic similarity between mayfly abdominal gills and wing pads reflects structural homology (shared evolutionary origin of the organs) or co-option of a conserved gene-regulatory module onto non-homologous outgrowths.

References

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