Abstract Gills are a feature of many aquatic animals, serving to extract oxygen from the water and to maintain ionic balance between the bloodstream and the environment. While gills first arose in early multicellular animals, their great diversity of forms make it unclear the extent to which they represent a continuously evolving structure or an example of convergent evolution. In chordates including vertebrates, gill filaments develop as outgrowths of epithelia, which also generate the gill slits and pores. The mesenchymal component derives from cranial neural crest cell progenitors in vertebrates and generates skeletal and connective tissues that support the gills and underlying vasculature. In this perspective, we discuss the evolutionary origins of gills in bilateria, the extent to which they are related to tentacles and other filamentous appendages, and how the repurposing of gill programs may have generated novel structures during the water to land transition, such as the book lungs of spiders and the outer ear and epiglottis of mammals. The gill filaments and gill-like tentacles of diverse marine invertebrates also frequently share a distinct type of cellular cartilage reminiscent of the elastic cartilage in vertebrate gill filaments and outer ears, suggesting that cartilage may have first arisen in gill-like structures of early bilateria. Elastic cartilage of vertebrates may therefore represent a vestige of invertebrate cartilage that pre-dates the vertebrate-specific hyaline cartilage of endochondral bones. We also discuss the possibility that the Dlx-expressing pharyngeal arches of vertebrates reflect elaborations of invertebrate gill and tentacle appendages that expressed the Dlx homolog distalless, with the gill filament elastic cartilage and gill-support endochondral bones deriving from distinct domains of the same Dlx-positive arches. These studies point to ancestral gills as a potentially rich source of morphological innovations across deep evolutionary time.
Thiruppathy et al. (Fri,) studied this question.