Photophore Morphogenesis and Extraocular Encephalopsin Expression during the Embryogenesis of Smalleye Pygmy Shark (Squaliolus aliae)

Abstract

Bioluminescence is a common phenomenon in marine organisms, especially in deep water where faint blue light remains. Among elasmobranchs, three families display the ability to emit light, the Etmopteridae, the Dalatiidae, and the Somniosidae. Luminous sharks have thousands of minute light organs, called photophores, that are mainly present ventrally and produce light. The main function of shark luminescence is counterillumination to camouflage the shark silhouette by mimicking the residual ambient light and avoiding being spotted by predators underneath. To perform counterillumination efficiently, luminescence needs to be finely adjusted. A new type of control was recently demonstrated via extraocular photoreception at the level of the light organ. An encephalopsin (i.e., opsin 3) was shown to be expressed in the vicinity of the photophore of an Etmopteridae species, Etmopterus spinax. This opsin was also demonstrated to be expressed concomitantly with the photophore development (i.e., when photophores become able to produce light) during E. spinax embryogenesis. To understand the photophore morphogenesis of different shark families, we analyzed the smalleye pygmy shark, Squaliolus aliae, with a photophore formation which represents the first report on the Dalatiidae family. Since Dalatiidae and Etmopteridae are phylogenetically closely related, the photophore morphogenesis was compared with an Etmopteridae representative, Etmopterus spinax. The results also reveal that Squaliolus aliae shares similar encephalopsin expression pattern as in Etmopterus spinax, which further supports evolutionary conservation of photophore morphogenesis as well as its own encephalopsin-based light perception across the two luminous shark families.