Homeosis in a scorpion supports a telopodal origin of pectines and components of the book lungs

Zhiyong Di, Gregory D. Edgecombe, Prashant P. Sharma

The morphological and functional evolution of appendages has played a key role in the diversification of arthropods. While the ancestral arthropod appendage is held to be polyramous, terrestriality is associated with the reduction or loss of appendage rami, which may obscure the homology of different appendage derivatives. Proxies for appendage homology have included surveys of cross-reactive antibodies for wing markers like Nubbin/PDM, which have suggested that the abdominal appendages of arachnids (e.g., book lungs, tracheal tubules) are derived from ancestral gills (epipods). Here, we discovered a rare case of inferred homeosis in a scorpion in which the bilobed genital opercula and the pectines are transformed to walking legs, and an abnormal sternite shows a book lung close to an everted structure comparable to the morphology of some Palaeozoic scorpion fossils. The observed morphology is consistent with abnormal expression of homeotic genes during embryonic development. The phenotype of this abnormal specimen suggests that the genital opercula, the pectines, and parts of the book lung may be derived from the telopodite of abdominal appendages rather than from epipods. This interpretation contradicts the "ancestral gill" hypothesis but reconciles features of the Palaeozoic scorpion fossil record with the embryology of modern scorpions.