Abstract

In most vertebrates, pharyngeal arches form in a stereotypic anterior-to-posterior progression. To gain insight into the mechanisms underlying evolutionary changes in pharyngeal arch development, here we investigate embryos and larvae of bichirs. Bichirs represent the earliest diverged living group of ray-finned fishes, and possess intriguing traits otherwise typical for lobe-finned fishes such as ventral paired lungs and larval external gills. In bichir embryos, we find that the anteroposterior way of formation of cranial segments is modified by the unique acceleration of the entire hyoid arch segment, with earlier and orchestrated development of the endodermal, mesodermal, and neural crest tissues. This major heterochronic shift in the anteroposterior developmental sequence enables early appearance of the external gills that represent key breathing organs of bichir free-living embryos and early larvae. Bichirs thus stay as unique models for understanding developmental mechanisms facilitating increased breathing capacity.

Highlights

  • The vertebrate pharynx is composed of a series of repeated embryonic structures called pharyngeal arches (Graham, 2008; Grevellec and Tucker, 2010)

  • Accelerated and predominant hyoid neural crest stream supplies bichir external gills To gain insights into the accelerated development of the hyoid segment, we focused on the cranial neural crest that arises from the closing neural folds

  • Cranial neural crest cells emerge in a characteristic pattern and split into mandibular, hyoid, and branchial streams, which in most vertebrates arise in a sequential anteroposterior order of appearance

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Summary

Introduction

The vertebrate pharynx is composed of a series of repeated embryonic structures called pharyngeal arches (Graham, 2008; Grevellec and Tucker, 2010). Sequential formation of pharyngeal segments represents a fundamental aspect of the metameric organization of the head and face (Piotrowski and Nusslein-Volhard, 2000; Couly et al, 2002; Choe and Crump, 2015). Any modifications of this well-established anteroposterior differentiation scheme would represent a radical alteration in development of the stereotypic chordate bauplan (Square et al, 2017)

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