A shared role for sonic hedgehog signalling in patterning chondrichthyan gill arch appendages and tetrapod limbs

Chondrichthyans (sharks, skates, rays and holocephalans) possess paired appendages that project laterally from their gill arches, known as branchial rays. This led Carl Gegenbaur to propose that paired fins (and hence tetrapod limbs) originally evolved via transformation of gill arches. Tetrapod limbs are patterned by a sonic hedgehog (Shh)-expressing signalling centre known as the zone of polarising activity, which establishes the anteroposterior axis of the limb bud and maintains proliferative expansion of limb endoskeletal progenitors. Here, we use loss-of-function, label-retention and fate-mapping approaches in the little skate to demonstrate that Shh secretion from a signalling centre in the developing gill arches establishes gill arch anteroposterior polarity and maintains the proliferative expansion of branchial ray endoskeletal progenitor cells. These findings highlight striking parallels in the axial patterning mechanisms employed by chondrichthyan branchial rays and paired fins/limbs, and provide mechanistic insight into the anatomical foundation of Gegenbaur's gill arch hypothesis.This research was supported by a Royal Society University Research Fellowship [UF130182 to JAG], by Plum foundation John E. Dowling and Laura and Arthur Colwin Endowed Summer Research Fellowships at the Marine Biological Laboratory to JAG, by a grant from the University of Cambridge Isaac Newton Trust to [14.23z to JAG], and by a grant from the Natural Sciences and Engineering Research Council of Canada [A5056 to BKH].This is the final version of the article. It first appeared from The Company of Biologists via http://dx.doi.org/10.1242/dev.13388