Abstract

Despite the wide variety of adaptive modifications in oral and branchial region of vertebrates, their early oropharyngeal development is considered rather uniform. From anterior to posterior, it comprises sequential formation of mouth and pharyngeal pouches, but the precise germ layer interactions have been studied on a limited number of model organisms so far. We have collected and analysed a complete series of embryonic stages of African bichir, American gar, and European sturgeon, representatives of three most basal (non-teleost) fish lineages. In all these species the standard vertebrate setting of foregut development is preceded by a unique process of anterior foregut expansion which gives rise to a distinct “pre-oral gut”. This pre-oral gut epithelia eventually extend to the external head surface where they contribute to various facial structures, including lips, sensory barbels and cement glands. This represents a first example of endodermal contribution to external head structures in vertebrates. Based on our analysis we conclude that this mode of foregut formation might be ancestral to all ray-finned fishes and has been lost only secondarily in teleosts due to the radical changes in their early embryonic development. Moreover, similar developmental processes described in tunicates and cephalochordates suggest that the evolutionary origin of the pre-oral gut might be nested even deeper in chordate history.