Exceptional diversity of opsin expression patterns inNeogonodactylus oerstedii(Stomatopoda) retinas

Abstract

Stomatopod crustaceans possess some of the most complex animal visual systems, including at least 16 spectrally distinct types of photoreceptive units (e.g., assemblages of photoreceptor cells). Here we fully characterize the set of opsin genes expressed in retinal tissues and determine expression patterns of each in the stomatopod Neogonodactylus oerstedii. Using a combination of transcriptome and RACE sequencing, we identified 33 opsin transcripts expressed in each N. oerstedii eye, which are predicted to form 20 long-wavelength–sensitive, 10 middle-wavelength–sensitive, and three UV-sensitive visual pigments. Observed expression patterns of these 33 transcripts were highly unusual in five respects: 1) All long-wavelength and short/middle-wavelength photoreceptive units expressed multiple opsins, while UV photoreceptor cells expressed single opsins; 2) most of the long-wavelength photoreceptive units expressed at least one middle-wavelength–sensitive opsin transcript; 3) the photoreceptors involved in spatial, motion, and polarization vision expressed more transcripts than those involved in color vision; 4) there is a unique opsin transcript that is expressed in all eight of the photoreceptive units devoted to color vision; and 5) expression patterns in the peripheral hemispheres of the eyes suggest visual specializations not previously recognized in stomatopods. Elucidating the expression patterns of all opsin transcripts expressed in the N. oerstedii retina reveals the potential for previously undocumented functional diversity in the already complex stomatopod eye and is a first step toward understanding the functional significance of the unusual abundance of opsins found in many arthropod species’ visual systems.

Neuroanatomy of stomatopod central complexes offers putative neural substrate for oriented behaviors in crustaceans

“…These connections are retinotopic, and part of the parallel pathways that relay sky-compass information, specifically polarization information, from the dorsal rim area (DRA) of the compound eye to the central complex. Although an analogous dorsal rim area has not been definitively identified in stomatopod crustaceans, molecular studies suggest that the ommatidia in the dorsal margin of N. oerstedii eyes, which have visual axes that generally face upwards, have a unique opsin expression pattern (Porter et al, 2020).…”

“…Although an analogous dorsal rim area has not been definitively identified in stomatopod crustaceans, molecular studies suggest that the ommatidia in the dorsal margin of N. oerstedii eyes, which have visual axes that generally face upwards, have a unique opsin expression pattern (Porter et al, 2020).…”

Stark trade-offs and elegant solutions in arthropod visual systems

“…Wavelength specificity typically originates from visual pigments, such as opsin-retinal-based chromophore pairs (see Box 2), which are relatively well understood across the animal kingdom. Studies over the past few decades have revealed the great diversity of these visual pigments (Porter et al, 2020(Porter et al, , 2012, with sensitivities that cover the visible as well as the UV spectral region (Briscoe and Chittka, 2001). The number of receptor types ranges from two in insects such as cockroaches, ants and many crustaceans to 12 in stomatopods (mantis shrimp) (Kelber, 2006).…”

The diversity of opsins in Lake Baikal amphipods (Amphipoda: Gammaridae)

“…Many mantis shrimps (Stomatopoda) species express multiple SWS, MWS, and LWS opsins in their retinas [ 10 , 29 ], even though monochromatic species with only LWS opsins are also known [ 30 ]. Studying expression patterns of the exceptionally diverse opsin transcripts in the stomatopod species Neogonodactylus oerstedii has revealed complex spatial patterns and is a promising approach towards understanding the functions of multiple opsins within one eye [ 29 ]. The model Euphausiacea species, Euphausia superba (Antarctic krill), expresses at least one LWS opsin and multiple MWS opsin transcripts [ 23 ].…”