Lifelong development of zebrafish gills: Asymmetries in early vascular patterning predict adult gill architecture

Gills are essential for fish respiration and have a highly specialized cellular architecture enabling efficient gas exchange. Surprisingly, the developmental processes underlying gill formation in zebrafish remain poorly understood. Here, we present for the first time a comprehensive analysis of the morphogenesis of gill arteries, filaments and lamellae during lifelong development. Our results provide important insights into the temporal and spatial pattern of gill angiogenesis, revealing fundamental differences in the formation of lateral versus medial filaments along the dorso-ventral axis. These early asymmetries correlate with, and likely underlie, the structural asymmetries observed in adult gills, which we quantitatively characterize. This indicates that a region-specific developmental programme establishes a blueprint for gill architecture maintained throughout life. We further show that lamellae develop through a complex interplay between endothelial and cranial neural crest-derived pillar cells. Notably, lamellar size, which strongly influences respiratory efficiency, depends on the position of the filament in the arch. Together, our work identifies key cellular and temporal mechanisms driving gill development and provides a framework to investigate broader principles of branching morphogenesis and angiogenesis in vertebrates.