Development of the zebrafish anterior lateral line system is influenced by underlying cranial neural crest

Abstract

The mechanosensory lateral line system of aquatic vertebrates comprises a superficial network of distributed sensory organs, the neuromasts, which are arranged over the head and trunk and innervated by lateral line nerves to allow detection of changes in water flow and pressure. While the well-studied zebrafish posterior lateral line has emerged as a powerful model to study collective cell migration, far less is known about development of the anterior lateral line, which produces the supraorbital and infraorbital lines around the eye, as well as mandibular and opercular lines over the jaw and cheek. Here we show that normal development of the zebrafish anterior lateral line system from cranial placodes is dependent on another vertebrate-specific cell type, the cranial neural crest. We find that cranial neural crest and anterior lateral lines develop in close proximity, with absence of neural crest cells leading to major disruptions in the overlying anterior lateral line system. Specifically, in the absence of neural crest neither supraorbital nor infraorbital lateral lines fully extend, such that the most anterior cranial regions remain devoid of neuromasts, while supernumerary ectopic neuromasts form in the posterior supraorbital region. Both neural crest and cranial placodes contribute neurons to the lateral line ganglia that innervate the neuromasts and in the absence of neural crest these ganglia, as well as the lateral line afferent nerves, are disrupted. Finally, we establish that as ontogeny proceeds, the most anterior supraorbital neuromasts come to lie within neural crest-derived frontal and nasal bones in the developing cranium. These are the same anterior supraorbital neuromasts that are absent or mislocated in specimens lacking neural crest cells. Together, our results establish that cranial neural crest and cranial placode derivatives function in concert over the course of ontogeny to build the complex cranial lateral line system.