Visual Gene Expression Reveals a cone-to-rod Developmental Progression in Deep-Sea Fishes

Abstract

Vertebrates use cone cells in the retina for colour vision and rod cells to see in dim light. Many deep-sea fishes have adapted to their environment to have only rod cells in the retina, while both rod and cone genes are still preserved in their genomes. As deep-sea fish larvae start their lives in the shallow, and only later submerge to the depth, they have to cope with diverse environmental conditions during ontogeny. Using a comparative transcriptomic approach in 20 deep-sea fish species from eight teleost orders, we report on a developmental cone-to-rod switch. While adults mostly rely on rod opsin (RH1) for vision in dim light, larvae almost exclusively express middle-wavelength-sensitive ("green") cone opsins (RH2) in their retinas. The phototransduction cascade genes follow a similar ontogenetic pattern of cone- followed by rod-specific gene expression in most species, except for the pearleye and sabretooth (Aulopiformes), in which the cone cascade remains dominant throughout development. By inspecting the whole genomes of five deep-sea species (four of them sequenced within this study: Idiacanthus fasciola, Chauliodus sloani; Stomiiformes; Coccorella atlantica, and Scopelarchus michaelsarsi; Aulopiformes), we found that deep-sea fish possess one or two copies of the rod RH1 opsin gene, and up to seven copies of the cone RH2 opsin genes in their genomes, while other cone opsin classes have been mostly lost. Our findings hence provide molecular evidence for a limited opsin gene repertoire and a conserved vertebrate pattern whereby cone photoreceptors develop first and rod photoreceptors are added only at later developmental stages.

Developmental changes of opsin gene expression in ray-finned fishes (Actinopterygii)

“…cone SWS1, SWS2, RH2, LWS and rod RH1 ), and detected a clear increase of GNAT1 : GNAT2 ratio with ageing, with the exception of the Aulopiformes deep-sea fishes. In this group, a rare discordance between the dominating opsin type (rod-specific) and phototransduction cascade genes (cone-specific) in adults suggests a presence of possibly transmuted photoreceptors, and an overall intriguing visual system which needs to be investigated further (Fig 3, Lupše et al 2021).…”

“…Functionally, rods generally allow for an improvement in visual acuity and startle responses in fishes (Fuiman 1993, Pankhurst et al 1993, Fuiman and Delbos 1998) and are also associated with motion sensitivity and the appearance of novel behaviours, such as schooling (Hunter & Coyne 1982). More specifically, higher rod expression increases individual performance of fishes living in the deep-sea (de Busserolles et al 2020, Lupše et al 2021). Additionally, laboratory experiments have shown that the ability to follow a rotating stripe pattern (the optomotor drum) might be dependent on rod formation and retinal development, as it is not seen in stages or specimens lacking rods (Blaxter 1986, Carvalho et al 2002, Magnuson et al 2020).…”

“…While the SWS1 is often missing from the genome or seen in one, at best two copies (Musilova et al, 2021) and SWS2 seen in up to three copies (Cortesi et al, 2015), teleost genomes can contain up to eight copies of RH2 (Musilova & Cortesi, 2021) and up to five copies of LWS (Cortesi et al, 2021). Unlike cone opsins, rod opsin duplicates are rarely found, most often in mesopelagic lineages (Pointer et al 2007, Musilova et al 2019a, Lupše et al 2021). Higher copy number is considered beneficial by providing more “substrate” for selection, as well as for alternative gene expression of the variants within the opsin type.…”

“…Photic conditions can change spatially and temporally, resulting in a visually heterogeneous environment in which visual systems of fishes are expected to be under natural selection that favours those that match the local environment (Carleton et al 2016). For example, longer and shorter wavelengths are scattered and filtered out with increasing water depth and consequently, fishes living in deep-water habitats such as sculpins of Lake Baikal (Hunt 1997), cichlids of lakes Malawi and Tanganyika (Sugawara et al 2005; Ricci et al 2022), and African crater lakes (Malinsky et al 2015; Musilova et al 2019b), as well as deep-sea fishes (Douglas et al 2003, Lupše et al 2021) have visual systems sensitive to the blue-green part of the visible spectrum. Adaptation can be achieved either through functional diversifications of opsin genes when mutations at key-spectral tuning sites shift the peak spectral sensitivity (λ max ) of the photopigment (Yokoyama 2008, 2020), or by regulation of the opsin gene expression.…”

Development of dim-light vision in the nocturnal coral reef fish family, Holocentridae

“…Contrastingly, in fishes which adopt dim environments, visual development seems to be characterised by a more rapid and extreme version of these changes. For example, some deep-sea fishes seem to possess cones as larvae but progress to having only rods in adulthood (Bozzano et al 2007;de Busserolles et al 2014a;Lupše et al 2021). However, most of the previous studies on visual development in dim environments focused on deep-sea fishes (Cortesi et al 2020).…”