Insects are the only arthropods to achieve powered flight, yet after more than a century of debate it remains unresolved when wings first evolved, from which ancestral structures they arose, and under what ecological and functional context the precursor structures were selected. The Devonian fossil record of insects is nearly empty and the oldest claimed Devonian insect (Rhyniognatha hirsti) has been questioned, so the earliest definitive winged fossils are no older than the Late Mississippian–Pennsylvanian (~325–310 Ma), while molecular divergence estimates place winged-insect origins far deeper — a long unobserved ghost range. Evo-devo (evolutionary developmental biology) and fossil evidence currently conflict between tergal (body-wall), leg-exite (gill-derived, later incorporated into the body wall), and dual-origin scenarios, with terrestrial gliding versus aquatic or semiaquatic respiratory original functions, and the weakly supported monophyly of Palaeoptera (mayflies plus dragonflies) still obscures which morphology is ancestral. This record audits the open problem of establishing the timing, anatomical precursors, and original function of the first insect wings.

Background

Insects (class Insecta, or Hexapoda in broad usage) are arthropods with a three-part body; the winged insects, or Pterygota, comprise nearly all described insect species and owe their radiation in large part to flight. Wings arose exactly once in the insect lineage: they are borne on the second and third thoracic segments of adults and develop as invaginated pads in the nymphs of hemimetabolous insects (insects with gradual metamorphosis, whose juveniles resemble adults). The immediate sister group of Pterygota is thought to be Zygentoma (silverfish), wingless insects, so the wing precursor must be sought in the lineage connecting wingless hexapods to the first winged insects.

Three classical hypotheses dominate the century-long debate on the anatomical origin of wings. The paranotal (or tergal) hypothesis derives wings from lateral expansions of the dorsal body wall (the tergum, plural terga), presumably used first for gliding. The exite (or epipod) hypothesis derives wings from an outgrowth of the leg — an exite — homologous to the gill-bearing epipods of crustaceans, which was later incorporated into the body wall; in its original aquatic reading this hypothesis implies gill-like, respiratory precursors. The dual origin hypothesis, revived by recent fossils and developmental data, holds that wings arose from a merger of tergal tissue and a leg-exite-derived pleural component (the pleuron being the lateral thoracic wall). Key fossil evidence includes Carboniferous nymphs preserving both thoracic wing pads and abdominal wing-like pads (Prokop et al. 2017, 2022), which support a dual model with serially repeated precursors. Key developmental evidence includes gene-knockout work using CRISPR (a targeted gene-editing technique) and gene-expression work in the crustacean Parhyale and in cockroaches and beetles (Bruce & Patel 2020; Clark-Hachtel & Tomoyasu 2020; Clark-Hachtel et al. 2021), which identifies leg-segment tissues qualified as wing homologues, and cricket wing-development work (Ohde et al. 2022) that instead supports a tergal origin — so the developmental evidence itself remains in conflict (reviewed by Ohde & Prokop 2025).

The phylogenetic frame is itself unsettled. The Palaeoptera — Ephemeroptera (mayflies) and Odonata (dragonflies and damselflies), whose adults cannot fold the wings back over the abdomen, in contrast to Neoptera, which can — may or may not be a clade. The competing topologies are Palaeoptera (mayflies + dragonflies), Metapterygota (dragonflies + Neoptera, all other winged insects), and Chiastomyaria (mayflies + Neoptera); a reanalysis of phylogenomic data (Simon et al. 2018) found overall molecular support for Palaeoptera but substantial hidden conflicting signal, and concluded the question remains open. Which topology is correct determines which extant lineage's morphology best approximates the ancestral winged insect (the protopterygote) and thus polarizes inference about wing precursors.

Timing is the least constrained dimension. The Devonian (419–359 Ma) insect record is nearly empty: the celebrated Rhyniognatha hirsti from the ~400 Ma Rhynie Chert, interpreted by Engel & Grimaldi (2004) as an insect with dicondylic (double-jointed) mandibles implying an already-winged stage, was restudied with 3D imaging by Haug & Haug (2017), who found the structures do not support insect affinity and may indicate a myriapod (centipede relative). Earliest definitive winged insects therefore appear only in the Late Mississippian–Pennsylvanian (~325–310 Ma), whereas large-scale phylogenomic dating (divergence-time inference from genome-scale sequence data; Misof et al. 2014) places insect origins near 479 Ma and pterygote stem divergences far earlier than any wing fossil. The origin of wings thus falls in a long unobserved ghost range, and current inferences about the protopterygote are extrapolated from Carboniferous fossils tens of millions of years after the event (e.g., the thoracic morphology of Eubleptus, a member of the extinct Paleozoic order Palaeodictyoptera, Prokop et al. 2026). Whether the ancestral lineage was terrestrial (Wipfler et al. 2019) or aquatic/semiaquatic with gill-like serial outgrowths serving a respiratory function (Prokop et al. 2023) is still actively debated and determines the plausible selective regime for the earliest wing precursors.

Problem Statement

Establish when insect wings first evolved, from which ancestral structures, and in what ecological and functional context. Concretely, the open problem asks for a historically accurate reconstruction of the origin of the Pterygota that resolves, as jointly consistent pieces of one explanation: (a) the timing of the first wings — in particular whether wing origins fall within the currently fossil-empty Devonian-to-early-Carboniferous ghost range (the unobserved interval between molecular divergence estimates and the oldest fossils) implied by molecular divergence estimates or close to the Late Mississippian–Pennsylvanian (~325–310 Ma) first appearance of definitive winged insects; (b) the anatomical identity of the wing precursor in the protopterygote lineage — lateral expansions of the dorsal body wall (paranota), an outer branch of the ancestral leg (a leg exite or epipod, homologous to the gill-bearing epipods of crustaceans) later incorporated into the body wall, a dual merger of tergal and pleural (lateral thoracic wall, leg-derived) tissues, or an explicitly specified variant or combination of these candidates — a question on which fossil, comparative-morphological, and developmental-genetic evidence currently conflict and must be weighed; and (c) the original function and selective regime of the precursor structures (aerodynamic gliding in a terrestrial lineage, respiration, or surface use in an aquatic or semiaquatic lineage, or an explicitly specified variant or combination of these). The unresolved topology at the base of the winged insects — Palaeoptera (Ephemeroptera, mayflies + Odonata, dragonflies and damselflies) monophyly versus Metapterygota (dragonflies + all other winged insects) or Chiastomyaria (mayflies + all other winged insects) — is retained as instrumental context needed to polarize the ancestral-state inference in (b) and (c), not as an independent deliverable of the reconstruction. An answer is complete when the timing, precursor, and functional claims are mutually consistent and robust to the currently conflicting developmental (tergal versus leg-exite/dual) and ecological (terrestrial versus aquatic) evidence — that is, when the answer commits to one preferred option for each of (a) the timing, (b) the precursor identity, and (c) the original function; names, for each commitment, the fossil, comparative-morphological, developmental-genetic, and phylogenetic evidence that discriminates the chosen option from the alternatives; and treats a finding that the evidence is currently insufficient to decide a sub-question as not by itself resolving that sub-question, so that any such finding must still be paired with the best-supported option for that sub-question.

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