Parallels in leg and wing proximal-distal patterning in Diptera and Lepidoptera

Abstract

Both insect wings and legs are appendages with a proximal-distal (PD) axis that is patterned during development, likely through a shared mechanism. Comparisons between the two types of appendages have been detailed in Drosophila melanogaster, a derived insect where both traits develop initially as imaginal discs. Here, we visualise and compare the expression of prominent PD developmental genes in the embryonic legs and larval wings of a lepidopteran species, Bicyclus anynana. We examine the domains of twelve appendage patterning genes that subdivide legs into distal, medial, or proximal domains (homothorax, extradenticle, teashirt, dachshund, Distal-less, spineless, rotund, bric-a-brac, Bar, aristaless, Lim, and apterous), two genes that refine the PD axis after initial specification in both legs and wings (fringe, brother of odd with entrails limited), and three morphogens (wingless, decapentaplegic, and vein). Our results reveal high spatial congruence in the order of PD gene expression between the two appendages providing evidence for a partially co-opted leg-PD-patterning network during wing evolution. Notably, we observe a distinct loss of the medial domain in the Bicyclus wing compared to the leg, supported by the absence of broad dachshund expression, as also observed in flies. Further comparisons with Drosophila highlight additional conserved versus lineage-specific regulatory architectures. These findings suggest a deeply conserved PD patterning logic across Mecopterida, while pointing to divergent mechanisms that likely facilitated the morphological innovation of insect wings.