A system to decipher the origins and relationships of all arthropod outgrowths

Abstract

Arthropods (insects, "crustaceans", myriapods, and chelicerates) display a fascinating diversity of ectodermal structures like plates, horns, helmets, knobs, carapaces, mimicry outgrowths, and wings. The origins and relationships of these structures has tantalized researchers for over a century: did these structures arise de novo in each lineage, or do they emerge from shared, ancestral primordia present in some or even all arthropods? One way to begin answering this is to assess the position and context of these structures on arthropod bodies: do these structures emerge from proximal embryonic leg segments that were converted into the body wall, or do they represent dorsal, non-leg-derived structures? Here, the expression of pannier, araucan, and drumstick - genes previously shown to distinguish proximal leg segments in crustaceans and insects - are examined in a chelicerate representative, the tarantula Acanthoscurria. This gene expression comparison, together with over a century of gene functional, morphological, embryological, and paleontological data, suggests that all arthropod leg segments correspond to each other in a one-to-one fashion, but that in many arthropod lineages, the base of the ancestral leg in the embryo flattens and expands to form the body wall of the adult. This would mean that many arthropod outgrowths which appear to stand on the lateral body wall, such as wings, tergal plates, and gin traps, are derived from the ancestral/embryonic leg base, and likely arose from shared, ancestral primordia present on this leg base in all arthropods. The analysis detailed here means that a simple three- or four-gene in situ expression experiment with pannier, araucan, and drumstick can elucidate the homologies of any arthropod ectodermal structure of interest, including beetle horns, treehopper helmets, and more.