Evolution and developmental diversity of skin spines in pufferfish

Abstract

Teleost fishes develop a huge variety of skin ornaments. How these diverse skin structures develop in fishes is unknown. The teleost fish order Tetraodontiformes includes some of the most unusual fishes such as the ocean sunfish, triggerfish and pufferfish, and they all can develop a vast assortment of scale derivatives that cover their bodies. Pufferfish have some of the most extreme scale derivatives, dermal spines, which are erected during their characteristic puffing behavior. Here we show that pufferfish spines develop through conserved gene interactions essential for other vertebrate skin appendage formation, like hair and feathers. However, pufferfish spines form without EDA (ectodysplasin), an essential molecule for the development of most vertebrate skin appendages. Modifying signaling pathways lead to loss or reduction of spine coverage in pufferfish, suggesting a mechanism for skin appendage diversification. We suggest that pufferfish skin spines evolved from a basic teleost scale-type through derived gene network modification in Tetraodontiformes.