This review presents a synthesis of shark bioluminescence knowledge. Up to date, bioluminescent sharks are found only in Squaliformes, and specifically in Etmopteridae, Dalatiidae and Somniosidae families. The state-of-the-art knowledge about the evolution, ecological functions, histological structure, the associated squamation and physiological control of the photogenic organs of these elusive deep-sea sharks is presented. Special focus is given to their unique and singular hormonal luminescence control mechanism. In this context, the implication of the photophore-associated extraocular photoreception—which complements the visual adaptations of bioluminescent sharks to perceive residual downwelling light and luminescence in dim light environment—in the hormonally based luminescence control is depicted in detail. Similarities and differences between shark families are highlighted and support the hypothesis of an evolutionary unique ancestral appearance of luminescence in elasmobranchs. Finally, potential areas for future research on shark luminescence are presented.

The velvet belly lanternshark (Etmopterus spinax) is a small deep-sea shark commonly found in the Eastern Atlantic and the Mediterranean Sea. This bioluminescent species is able to emit a blue-green ventral glow used in counter-illumination camouflage, mainly. In this study, paired-end Illumina HiSeq^TM technology has been employed to generate transcriptome data from eye and ventral skin tissues of the lanternshark. About 64 and 49 million Illumina reads were generated from skin and eye tissues respectively. The assembly allowed us to predict 119,749 total unigenes including 94,569 for the skin transcriptome and 94,365 for the eye transcriptome while 74,753 were commonly found in both transcriptomes. A taxonomy filtering was applied to extract a reference transcriptome containing 104,390 unigenes among which 38,836 showed significant similarities to known sequences in NCBI non-redundant protein sequences database. Around 58% of the annotated unigenes match with predicted genes from the Elephant shark (Callorhinchus milii) genome. The transcriptome completeness has been evaluated by successfully capturing around 98% of orthologous genes of the « Core eukaryotic gene dataset » within the E. spinax reference transcriptome. We identified potential “light-interacting toolkit” genes including multiple genes related to ocular and extraocular light perception processes such as opsins, phototransduction actors or crystallins. Comparative gene expression analysis reveals eye-specific expression of opsins, ciliary phototransduction actors, crystallins and vertebrate retinoid pathway actors. In particular, mRNAs from a single rhodopsin gene and its potentially associated peropsin were detected in the eye transcriptome, only, confirming a monochromatic vision of the lanternshark. Encephalopsin mRNAs were mainly detected in the ventral skin transcriptome. In parallel, immunolocalization of the encephalopsin within the ventral skin of the shark suggests a functional relation with the photophores, i.e. epidermal light-producing organs. We hypothesize that extraocular photoreception might be involved in the bioluminescence control possibly acting on the shutter opening and/or the photocyte activity itself. The newly generated reference transcriptome provides a valuable resource for further understanding of the shark biology.

In the darkness of the ocean, an impressive number of taxa have evolved the capability to emit light. Many mesopelagic organisms emit a dim ventral glow that matches with the residual environmental light in order to camouflage themselves (counterillumination function). Sharks use their luminescence mainly for this purpose. Specific lateral marks have been observed in Etmopteridae sharks (one of the two known luminous shark families) suggesting an inter/intraspecific recognition. Conversely, dorsal luminescence patterns are rare within these deep-sea organisms. Here we report evidence that Etmopterus spinax, Etmopterus molleri and Etmopterus splendidus have dorsal luminescence patterns. These dorsal patterns consist of specific lines of luminous organs, called photophores, on the rostrum, dorsal area and at periphery of the spine. This dorsal light seems to be in contrast with the counterilluminating role of ventral photophores. However, skin photophores surrounding the defensive dorsal spines show a precise pattern supporting an aposematism function for this bioluminescence. Using in situ imaging, morphological and histological analysis, we reconstructed the dorsal light emission pattern on these species, with an emphasis on the photogenic skin associated with the spine. Analyses of video footage validated, for the first time, the defensive function of the dorsal spines. Finally, we did not find evidence that Etmopteridae possess venomous spine-associated glands, present in Squalidae and Heterondontidae, via MRI and CT scans. This work highlights for the first time a species-specific luminous dorsal pattern in three deep-sea lanternsharks. We suggest an aposematic use of luminescence to reveal the presence of the dorsal spines. Despite the absence of venom apparatus, the defensive use of spines is documented for the first time in situ by video recordings.

Bioluminescence is a widespread phenomenon in the marine environment. Among luminous substrates, coelenterazine is the most widespread luciferin, found in more than nine phyla. The wide phylogenetic coverage of this light-emitting molecule has led to the hypothesis of its dietary acquisition that was demonstrated in one cnidarian and one lophogastrid shrimp species so far. Within Ophiuroidea, the dominant class of luminous echinoderms, Amphiura filiformis is a model species known to use coelenterazine as substrate of a luciferin / luciferase luminous system. The aim of this study was to perform a long-term monitoring of A. filiformis luminescent capabilities during captivity. Our results show (i) depletion of luminescent capabilities within five months when the ophiuroid is fed with a coelenterazine-free diet and (ii) a quick recovery of luminescent capabilities when the ophiuroid is fed with coelenterazine-supplemented food. The present work demonstrates for the first time a trophic acquisition of coelenterazine in A. filiformis to maintain light emission capabilities.