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Gegenbaur's classical hypothesis of jaw-gill arch serial homology is widely cited, but remains unsupported by either palaeontological evidence (for example, a series of fossils reflecting the stepwise transformation of a gill arch into a jaw) or developmental genetic data (for example, shared molecular mechanisms underlying segment identity in the mandibular, hyoid and gill arch endoskeletons). Here we show that nested expression of Dlx genes--the 'Dlx code' that specifies upper and lower jaw identity in mammals and teleosts--is a primitive feature of the mandibular, hyoid and gill arches of jawed vertebrates. Using fate-mapping techniques, we demonstrate that the principal dorsal and ventral endoskeletal segments of the jaw, hyoid and gill arches of the skate Leucoraja erinacea derive from molecularly equivalent mesenchymal domains of combinatorial Dlx gene expression. Our data suggest that vertebrate jaw, hyoid and gill arch cartilages are serially homologous, and were primitively patterned dorsoventrally by a common Dlx blueprint.

The paratympanic organ, a mechanosensory hair cell-containing pouch in the amniote middle ear, was first described 100 years ago, yet its origins remain unresolved. Homology with the anamniote spiracular organ is supported by association with homologous skeletal elements and similar central targets of afferent neurons, suggesting it might be a remnant of the water-dependent lateral line system, otherwise lost during the amniote transition to terrestrial life. However, this is incompatible with studies suggesting that it arises from the first epibranchial (geniculate) placode. Here we show that a previously undiscovered Sox2-positive placode, immediately dorsal to the geniculate placode, forms the paratympanic organ and its afferent neurons, which are molecularly and morphologically distinct from geniculate neurons. These data remove the only obstacle to accepting the homology of the paratympanic organ and spiracular organ. We hypothesize that the paratympanic organ/spiracular organ represents an ancient head ectoderm module, developmentally and evolutionarily independent of both lateral line and epibranchial placodes.

Electroreception is an ancient subdivision of the lateral line sensory system, found in all major vertebrate groups (though lost in frogs, amniotes and most ray-finned fishes). Electroreception is mediated by 'hair cells' in ampullary organs, distributed in fields flanking lines of mechanosensory hair cell-containing neuromasts that detect local water movement. Neuromasts, and afferent neurons for both neuromasts and ampullary organs, develop from lateral line placodes. Although ampullary organs in the axolotl (a representative of the lobe-finned clade of bony fishes) are lateral line placode-derived, non-placodal origins have been proposed for electroreceptors in other taxa. Here we show morphological and molecular data describing lateral line system development in the basal ray-finned fish Polyodon spathula, and present fate-mapping data that conclusively demonstrate a lateral line placode origin for ampullary organs and neuromasts. Together with the axolotl data, this confirms that ampullary organs are ancestrally lateral line placode-derived in bony fishes.