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.

Evolutionary Conservation of Photophore Ultrastructure in Sharks: The Case of a Dalatiid Squalomorph

“…The vesicular and granular areas appear distinct but do not appear delimited by a membrane. Contrary to previous studies on the Dalatiidae and Etmopteridae [11,21,26,[31][32][33][34], the ultrastructure The present TEM analysis of D. licha photophore morphology shows they are composed of an iris-like structure (ILS) associated with a spherical pigmented sheath encompassing one unique regionalized photocyte (Figure 4). The basal zone of the photocyte contains a granular area filled with a large acidophilic secretion and granular inclusions.…”

“…The general morphology of photophore was also investigated in a few other species (i.e., Isistius brasiliensis and Dalatias licha): a round-shaped organ composed of a single photocyte embedded in a pigmented sheath and surmounted by lens cells [26,33]. The photophore morphogenesis during the embryogenesis of Squaliolus aliae follows the same four steps as the development of photophores in Etmopterus spinax [34]. The morphology of the Zameus photophore is similar to that of the light organ of dalatiids [22].…”

A brittle star is born: Ontogeny of luminous capabilities in Amphiura filiformis

“…filiformis [ 53 ]. The hypothesis of coevolution of light emission and perception is strongly suggested in marine bioluminescent organisms [ 43 , 54 – 57 ]. The inability to produce light for the early pluteus stage follows the transcriptomic data showing that the early pluteus (64 hours post-fertilization) lacks photoreceptive proteins [ 52 ].…”

“…The colocalized luciferase expression with the non-visual opsin in the arm's spines led to the hypothesis this opsin plays a role in a photoemission-perception process regulating the amount of light produced in A. filiformis [53]. The hypothesis of coevolution of light emission and perception is strongly suggested in marine bioluminescent organisms [43,[54][55][56][57]. The inability to produce light for the early pluteus stage follows the transcriptomic data showing that the early pluteus (64 hours post-fertilization) lacks photoreceptive proteins [52].…”

“…Other studies are more related to the ontogenic morphological development of light organs. Morphogenesis of luminous symbiotic organs was performed in organisms such as Euprymna scolopes, Sagamichthys schnakenbecki, and Nuchequula nuchalis [37][38][39], while few studies have been conducted on light organ development in intrinsic light emitters such as Porichthys notatus, Etmopterus spinax, and Squaliolus aliae [40][41][42][43]. Those few studies led to real comparison difficulties since they followed only proxies of luminous capabilities emergence during the ontogeny of organisms endowed with several luminous systems.…”