Caudal fin shape imprinted during late zebrafish embryogenesis is re-patterned by SONIC hedgehog

Abstract

Appendage shape is formed during development - and re-established during regeneration - according to spatial and temporal cues that orchestrate local cell behaviors. The caudal fin is the primary appendage used for propulsion in most fishes, and the organ exhibits a range of distinct morphologies adapted for different swimming strategies. Zebrafish caudal fins develop with a forked shape, with longer supportive bony rays at the periphery and shorter rays at the center of the external organ. Here, we show that inducing a transient pulse of sonic hedgehog a (shha) overexpression during late embryonic development leads to excess growth of the central rays, causing the adult caudal fin to grow into a triangular, truncate shape. Our results identify a period - prior to endogenous shha expression and before differentiation of skeletogenic cells in these tissues - during which the imprinted fin shape can be re-patterned by hyper-physiological Shh stimulation. After this critical developmental period, overexpression of shha does not alter the shape of the adult caudal fin. Both global and local ectopic shha overexpression during the critical window of embryogenesis are sufficient to alter the adult fin shape, and a normal forked shape can be rescued by subsequent treatment with an antagonist of the canonical Shh pathway. The early pulse of shha expands hox13 expression domains in the fin primordium, and leads to excessive proliferation in the central regions of the fin. After developing with a truncate shape, the truncate morphology was remembered and rebuilt during regeneration, suggesting that the shape imprinted during embryogenesis informs both development and regenerative morphogenesis. Ray-finned fishes have evolved a wide spectrum of caudal morphologies, and the current work offers insights into the developmental time periods and processes that inform growth and ultimate shape of the fin.