Whether insect wings are transformed ancestral crustacean leg exites (outer lateral leg branches), novel body-wall outgrowths, or mergers of both remains one of the most debated questions in evolutionary developmental biology. CRISPR–Cas9 knockouts of leg-patterning genes in the amphipod crustacean Parhyale hawaiensis led Bruce and Patel (2020) to propose that two proximal leg segments of the ancestral pancrustacean were incorporated into the insect body wall, carrying a precoxal leg exite onto the back where it became the wing. This problem asks researchers to test that alignment across the pancrustacean phylogeny (pancrustaceans are the clade comprising crustaceans together with hexapods, the six-legged arthropods, i.e., insects and their closest relatives) through comparisons with other arthropods more representative of the ancestral state, in which the hypothesized proximal leg region is not fused to the body wall — for example, crustacean lineages branching between Parhyale and insects, and early-diverging wingless insects. The gene regulatory network changes that redeployed and muscularized the exite into an articulated flight organ, together with the developmental-genetic mechanism of the segment incorporation itself, remain related open questions whose resolution would deepen the mechanistic reconstruction but is not required to answer the homology question. A well-supported refutation of the exite alignment, in favor of tergal or dual-origin alternatives, equally resolves the question.

Background

Insects are the only winged arthropods and make up roughly three-quarters of described animal species, so the evolutionary origin of their wings has been contested for more than a century. Three frameworks dominate the debate. The paranotal (tergal) hypothesis derives wings from lateral expansions of the dorsal body wall (the tergum). The exite (epipodite) hypothesis derives wings from an exite — an outer lateral branch of an arthropod limb, such as the gill-bearing epipodite of aquatic crustaceans. Dual-origin models propose that tergal and leg-derived tissues merged into a single organ. A related classical idea, the subcoxal theory, holds that the proximal-most leg segments (the subcoxa or precoxa) of an ancestral arthropod were folded into the insect body wall, where they became the pleural plates that anchor the wings.

Problem Statement

Determine whether insect wings descend from an ancestral crustacean leg exite. Test the alignment proposed by Bruce and Patel (2020) — insect wings homologous to the proximal (precoxal) leg exite of the ancestral pancrustacean, with two ancestral proximal leg segments (the precoxa and the crustacean coxa) incorporated into the insect body wall — through comparisons between insects and other arthropods more representative of the ancestral state, in which the hypothesized proximal leg region is not fused to the body wall; crustacean lineages branching between Parhyale and the hexapods (the six-legged arthropods, i.e., insects and their closest relatives) and early-diverging wingless insects are examples of informative comparison targets. Do these comparisons show one consistent alignment of the wing with a specific ancestral leg outgrowth and segment-incorporation pattern, or do they falsify or modify it, including in favor of tergal or dual-origin alternatives? A well-supported refutation — evidence from such comparisons that wings are not homologous to the precoxal exite, or that an alternative alignment fits the data better — resolves the problem by settling the question. Related open questions whose resolution would deepen the reconstruction, but which are not conditions for resolving the homology problem, include the gene regulatory network changes — cis-regulatory (changes in the regulatory DNA that controls where and when genes act) and trans-acting (changes in the transcription factors and other diffusible regulators that bind such DNA) — that re-deployed and repositioned the ancestral exite within the body wall and converted a lateral leg lobe into a flat, articulated wing blade and hinge, distinguishing retained ancestral exite patterning from newly co-opted circuitry; and the developmental-genetic mechanisms by which the proximal leg segments were morphologically incorporated into the body wall, together with the associated changes in musculature and articulation.

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