Innervation Drives Postembryonic Expansion of the Zebrafish Anterior Lateral Line System

The lateral line system is an essential sensory modality used by fishes and aquatic amphibians to sense hydrodynamic information. The system comprises distributed sense organs called neuromasts and their afferent nerves, organized into anterior lateral lines around the eye and jaw and posterior lateral lines (LL) on the trunk. At postembryonic stages, early forming neuromasts expand in size and sink into bony canals, while late-forming superficial neuromasts are added as the fish grows. Unlike the well-studied zebrafish posterior LL, details of anterior LL postembryonic development remain unknown. Here, we have characterized developmental mechanisms and innervation patterns driving expansion of the zebrafish anterior LL. Using tissue-clearing to observe neuromast and nerve markers through ontogeny, we demonstrate continuous neuromast addition in the anterior LL, with peak rates at larval stages of 7-10 mm standard length (SL). Lines of superficial neuromasts form parallel to existing lines of presumptive canal neuromasts as late as 7 mm SL, with new neuromasts added through migration of new primordia, budding, intercalation, and a novel "hybrid-origin" mechanism. Despite some canal lines being innervated by the anterodorsal ganglion, all superficial lines are innervated by the anteroventral ganglion. Anterior LL ganglion ablation reveals that denervation abrogates superficial neuromast formation-including via the hybrid-origin mechanism-and reduces growth of canal neuromasts. While the anterior and posterior LL use disparate developmental mechanisms, innervation is critical to the expansion of both. Our findings reveal a "developmental switch" at 7 mm SL, when innervation becomes necessary for a secondary phase of anterior LL development.