Clark-Hachtel and Tomoyasu (2020) showed that a gene network resembling the insect wing gene network (the pre-wing gene network, preWGN) operates in two separate crustacean tissues of the amphipod Parhyale hawaiensis — the tergal (dorsal body wall) plates and the proximal leg segments — and proposed that both qualify as wing homologues, supporting a dual evolutionary origin of insect wings through a merger of two distinct tissues. The resulting question cluster remains open but has been substantially reframed by later work: current evidence converges on the idea that the lateral tergum itself derives from an incorporated proximal leg segment bearing an exite (an outer leg branch), yet which tissues (incorporated exite homolog, pleuron, medial tergum) contributed which morphological and genetic elements to the first wing, whether the shared preWGN reflects co-option, serial homology, or convergence, and the breadth of the preWGN across non-winged arthropods all remain unresolved, as the 2025 review by Ohde and Prokop confirms by naming tissue contributions the field's current focus.

Background

How insect wings arose is one of the longest-standing debates in evolutionary biology. Two hypotheses have competed since the nineteenth century. The paranotal (tergal) hypothesis derives the wing from fixed outgrowths of the dorsal body wall plate (the tergum); the exite hypothesis, revived by Averof and Cohen's (1997) expression data, derives it from a movable outer branch of the ancestral leg (an exite), homologous to crustacean gill/epipod structures. Niwa et al. (2010) gave the debate a developmental-genetic form: in the beetle Tribolium, two embryonic primordia — one tergal, one pleural (the body wall lateral to the leg base) — express the wing selector gene vestigial (vg) and physically merge into a single wing disc, suggesting the wing arose by integration of two developmental modules. A gene regulatory network (GRN, the set of regulatory genes and their interactions that builds a structure) including wingless (wg, a Wnt ligand), vg, apterousA (apA, specifying dorsal wing fate), and nubbin builds every insect wing. Clark-Hachtel and Tomoyasu (2020) asked where the ingredients of this network existed before wings: in the wingless crustacean Parhyale hawaiensis (an amphipod, sister-lineage context to insects), they found a network similar to the insect wing network — the pre-wing gene network, preWGN — operating in both the tergal plates and the proximal leg segments. They concluded that both tissues qualify, from an evo-devo standpoint, as candidate crustacean wing homologues, and argued this supports a dual evolutionary origin of wings: novelty through merger of two distinct tissues. A companion study, Bruce and Patel (2020), knocked out leg-patterning genes in Parhyale and proposed the opposite emphasis: insect wings and body walls both evolved from ancient proximal leg segments, a wing being the exite of a leg segment (the precoxa) that was incorporated into the body wall — implying the crustacean 'tergal' preWGN territory is itself leg-derived. Subsequent work sharpened the alternatives: Fisher et al. (2021) found that wing-network genes in the milkweed bug Oncopeltus pattern many bilayered cuticular body-wall outgrowths, reconceiving the wing network as a versatile general module for body-wall lobes; Clark-Hachtel et al. (2021) found both tergal-nature and pleural-nature wing-related tissues in cockroach wingless segments, but also vg-independent wing contributions and vg-dependent tissues that do not form wing tissue; Ohde et al. (2022) showed cricket wing blades grow from the lateral tergal margin — a margin that crustacean studies suggest contains a lateral subdomain of separate (proximal-leg-derived) evolutionary origin — via redeployment of a conserved vg-dependent feed-forward growth circuit involving Wnt, Fat-Dachsous (a cell-cell signalling pair controlling planar tissue growth), and Hippo (a growth-control kinase pathway) signaling; and Bruce and Patel (2022) argued the Daphnia carapace is a cryptically persisted serial homolog of that same exite-derived tissue, homologous to the Parhyale tergal plate and the insect wing. A 2025 review (Ohde and Prokop) synthesizes this into a working picture — an ancestral precoxa leg segment with an exite incorporated within the hexapod lateral tergum — while explicitly leaving open how much the incorporated exite homolog, the pleuron, and the medial 'bona fide' tergum each contributed to wing evolution. Homology judgments here rest on three kinds of evidence the field combines: gene expression and functional perturbation (CRISPR/Cas9 knockouts, RNA interference) across taxa, phylogenetic ancestry inference (ancestral polarity of a network across the arthropod tree), and the Paleozoic fossil record of lateral body outgrowths. Key concepts: serial homology (repeated structures sharing a developmental origin within one body plan, like wings and other segmental outgrowths), co-option (recruitment of an existing GRN into a new structure), and convergence (independent assembly of a similar network from a limited developmental toolkit).

Problem Statement

From the open questions raised by Clark-Hachtel & Tomoyasu (2020), the surviving open problem is a mechanistic and historical reconstruction of the origin of the insect wing from the pre-wing gene network (preWGN) evidence, in three linked parts. (1) Explain why a wing-like gene network operates in both the tergal plates and the proximal leg segments of crustaceans: determine whether this reflects co-option of the network from one tissue to the other, shared ancestry (serial homology) between the two tissues with retention of the network (as the accompanying incorporated-proximal-leg-segment account proposes), convergent deployment from a limited developmental toolkit (an alternative emphasized by later work, e.g., Fisher et al., 2021), or a combination, drawing on comparative functional (loss-of-function) and phylogenetic evidence of the kind the source treats as decisive for homology claims. (2) Establish which tissue(s) — the incorporated exite homolog within the lateral tergum, the pleuron, the medial bona fide tergum, and/or proximal leg tissues — contributed which morphological and genetic elements to the first wing, and identify the gene-regulatory changes (e.g., the source's proposed 'cross-wiring' of the two similar networks into a single fused ancestral wing GRN, and redeployment of network nodes) and their sequence/timing by which the contributing primordia were integrated into a single organ; this includes deciding whether a genuine merger of two distinct preWGN-bearing tissues occurred at all, as the dual-origin hypothesis states, or whether one tissue alone was transformed — the source itself calls the evolutionary route from the two sets of wing homologs to the bona fide insect wing 'still a mystery for future studies'. (3) Build the comparative evidence base needed for (1) and (2): identify tissues homologous to insect wings in lineages outside Insecta (additional crustaceans, apterygote hexapods, and outgroups) to establish the taxonomic breadth and ancestral polarity of the preWGN — information the source notes will be pivotal for resolving the mechanism and route questions — using comparative developmental and loss-of-function evidence, with cell-lineage data as one further available line of evidence. All three parts are jointly required: a resolution must commit to the best-supported answer among the alternatives posed in (1) and (2) — or, where the available evidence cannot discriminate among them, state explicitly that it is inconclusive and specify the decisive test that would settle it — and the comparative evidence base of (3), including its cell-lineage line of evidence, is itself a required part of the resolution, not merely a prerequisite for (1) and (2); for (3), building that base consists in compiling and evaluating the published comparative developmental, loss-of-function and cell-lineage evidence available across the named lineages — no new experimental data are required of the solver — and, where that evidence is silent, identifying the gap and the decisive observation or experiment that would close it.

References

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  2. Bruce, H. S. & Patel, N. H. (2020). Knockout of crustacean leg patterning genes suggests that insect wings and body walls evolved from ancient leg segments. Nature Ecology & Evolution 4, 1703–1712. DOI 10.1038/s41559-020-01349-0. https://doi.org/10.1038/s41559-020-01349-0
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