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The internal phylogeny of Chelicerata and the attendant evolutionary scenario of arachnid terrestrialization have a long and contentious history. Previous studies of developmental gene expression data have suggested that respiratory systems of spiders, crustaceans, and insects are all serially homologous structures derived from the epipods (outer appendage rami) of the arthropod ancestor, corresponding to an ancestral gill. A separate body of evidence has suggested that the respiratory systems of arachnids are modified, inverted telopods (inner rami, or legs). Here I review these dissonant homology statements and compare the developmental genetic basis for respiratory system development in insects and arachnids. I show that the respiratory primordia of arachnids are not positionally homologous to those of insects. I further demonstrate that candidate genes critical to tracheal fate specification in Drosophila melanogaster are expressed very differently in arachnid exemplars. Taken together, these data suggest that mechanisms of respiratory system development are not derived from homologous structures or mechanisms in insects and arachnids, and that different terrestrial arthropod lineages have solved the challenge of aerial respiration using different developmental mechanisms.

Chelicerates and the Conquest of Land: A View of Arachnid Origins Through an Evo-Devo Spyglass