Abstract :
[en] Echinoderms are an intriguing group of deuterostome invertebrates which have been known to be
sensitive to light despite lacking complex eye structures. They are therefore an interesting group
to study the evolution of light perception in metazoans. Previous studies on sea urchins, sea stars
and brittle stars have identified photoreceptors in various body parts, such as tube feet, spines, and
the nervous system (Ullrich-Lüter et al. 2011; 2013; Delroisse et al. 2014). Some studies also led
to the discovery of low-resolution spatial (but eye-less) vision in some species (Blevins et Johnsen
2004; Sumner-Rooney et al. 2020). The light perception abilities of holothuroids (sea cucumbers),
however, have been largely understudied, with some punctual results from ethological studies
(e.g., some species flee away from a light source while other species retract their oral tentacles
under strong light exposure) (Pople. 1958; Bonham & Held 1963 ; Dong et al. 2010, 2011). To
investigate photoreception in sea cucumbers, we used a multidisciplinary approach focusing on
opsins, which are prototypical photoreceptor proteins in bilaterians. Our analysis of genomes and
transcriptomes from multiple holothuroid species revealed six ancestral opsin types. The
expression of rhabdomeric opsins was specifically detected in photoreceptors located in the oral
tentacles, radial nerves, and tube feet in Holothuria forskali, a European species of the order
Holothuriida, suggesting well-developed extraocular photoreception in these animals. Our
investigation also focused on the order of Apodida, a group of sea cucumbers with elongated
bodies and lacking tube feet, in which some researchers have reported the presence of visual
structures at the root of their tentacles (Berrill 1965 ; Yamamoto et Yoshida 1978). Our study
demonstrated the expression of a ciliary opsin in the photo-sensory neuroepithelial structures of
the tropical species Euapta godeffroyi, which form eyespots at the base of each tentacle (figure
1A, B). A similar expression of opsins in the baso-tentacular nerves was observed in the small
European burrowing species Oestergrenia digitata. Additionally, we detected opsins in the
sensory cupules, which are structures located on the inner surface of tentacles and having unknown
sensory functions (figure 1C, D, E). Finally, our ethological tests on three holothuroid species
showed that they moved away from (Holothuria forskali and Euapta godeffroyi) or toward
(Synapta maculata) a light source, specifically for shorter wavelengths corresponding to blue and
green light. Turning the spotlights on these amazing sea cucumbers and more broadly on all
echinoderms is important to better understand the mechanisms and evolution of extraocular
photoreception in the deuterostome lineage
