The Origin of Vertebrate Gills

Pharyngeal gills are a fundamental feature of the vertebrate body plan [1]. However, the evolutionary history of vertebrate gills has been the subject of a long-standing controversy [2, 3, 4, 5, 6, 7, 8]. It is thought that gills evolved independently in cyclostomes (jawless vertebrates—lampreys and hagfish) and gnathostomes (jawed vertebrates—cartilaginous and bony fishes), based on their distinct embryonic origins: the gills of cyclostomes derive from endoderm [9, 10, 11, 12], while gnathostome gills were classically thought to derive from ectoderm [10, 13]. Here, we demonstrate by cell lineage tracing that the gills of a cartilaginous fish, the little skate (Leucoraja erinacea), are in fact endodermally derived. This finding supports the homology of gills in cyclostomes and gnathostomes, and a single origin of pharyngeal gills prior to the divergence of these two ancient vertebrate lineages.