From Scale to Spine: Evolution and Developmental Diversity of Skin Spines in Pufferfishes

Abstract

Teleost fishes develop a remarkable variety of skin ornaments. However, the developmental basis of these structures is poorly understood. The teleost order Tetraodontiformes includes diverse fishes such as the ocean sunfishes, triggerfishes and pufferfishes, which exhibit a vast assortment of scale derivatives. Pufferfishes and porcupine fishes possess some of the most extreme scale derivatives, dermal spines, which are erected during their characteristic puffing behavior. Here, we focus on pufferfishes and demonstrate that the spines develop through conserved gene interactions that underlie skin appendage formation throughout other vertebrates, including avian feathers and mammalian hair. Pufferfish spine development retains the conserved role of the EDA (ectodysplasin) signaling pathway, suggesting that EDA is an important molecule/pathway for the development of diverse vertebrate skin appendages, including these modified scale-less spines of the pufferfish lineage. Further modification of genetic signaling from both CRISPR-Cas9 and small molecule inhibition can lead to both loss or reduction of spine coverage in pufferfish, providing a mechanism for skin appendage diversification observed in the extant clade of pufferfishes (Tetraodontidae). Dermal spines are unique scale-derivatives that evolved through conserved gene network modification. In pufferfish they exhibit broad variation in coverage, enabling adaptation to diverse ecological niches.