South American Weakly Electric Fish (Gymnotiformes) Are Long-Wavelength-Sensitive Cone Monochromats

Abstract

Losses of cone opsin genes are noted in animals that are nocturnal or rely on senses other than vision. We investigated the cone opsin repertoire of night-active South American weakly electric fish. We obtained opsin gene sequences from genomic DNA of 3 gymnotiforms (Eigenmannia virescens, Sternopygus macrurus, Apteronotus albifrons) and the assembled genome of the electric eel (Electrophorus electricus). We identified genes for long-wavelength-sensitive (LWS) and medium-wavelength-sensitive cone opsins (RH2) and rod opsins (RH1). Neither of the 2 short-wavelength-sensitive cone opsin genes were found and are presumed lost. The fact that Electrophorus has a complete repertoire of extraretinal opsin genes and conservation of synteny with the zebrafish (Danio rerio) for genes flanking the 2 short-wavelength-sensitive opsin genes supports the supposition of gene loss. With microspectrophotometry and electroretinograms we observed absorption spectra consistent with RH1 and LWS but not RH2 opsins in the retinal photoreceptors of E. virescens. This profile of opsin genes and their retinal expression is identical to the gymnotiform's sister group, the catfish, which are also nocturnally active and bear ampullary electroreceptors, suggesting that this pattern likely occurred in the common ancestor of gymnotiforms and catfish. Finally, we noted an unusual N-terminal motif lacking a conserved glycosylation consensus site in the RH2 opsin of gymnotiforms, a catfish and a characin (Astyanax mexicanus). Mutations at this site influence rhodopsin trafficking in mammalian photoreceptors and cause retinitis pigmentosa. We speculate that this unusual N terminus may be related to the absence of the RH2 opsin in the cones of gymnotiforms and catfish.

Seeing the rainbow: mechanisms underlying spectral sensitivity in teleost fishes

“…Since the vertebrate common ancestor, some teleost lineages have gained additional opsin copies through duplications so that they now have more opsins than other vertebrates (Davies et al, 2012;Musilova et al, 2019a;Rennison et al, 2012). These extra copies are sometimes the result of the teleost-specific whole genome duplication (Escobar-Camacho et al, 2019a;Liu et al, 2016;Liu et al, 2019;Morrow et al, 2011), but can also result from duplications specific to particular lineages, e.g. the tandem duplications of the SWS2 and RH2 genes that are shared across Actinopterygians Parry et al, 2005).…”

“…In addition to gene duplication, opsins can also be lost from the genome. This may be the result of photoreceptor simplification in spectrally narrow environments or when light intensities change severely such as in the deep sea (Musilova et al, 2019a) or turbid waters (Escobar-Camacho et al, 2017;Lin et al, 2017;Liu et al, 2016;Weadick et al, 2012). These habitats are generally darker and have reduced levels of UV light (and red light, in the case of deeper waters; Fig.…”

Chromosome‐level assembly of southern catfish (silurus meridionalis) provides insights into visual adaptation to nocturnal and benthic lifestyles

“…In addition, as short wavelengths such as blue are more easily scattered by suspended particles, turbid water directly limits their transmission and reduces their depth of travel into the water (Spady et al, 2005). Therefore, the spectrum of ambient light is shifted toward the long-wavelength region and the spectral breadth of light available for vision is restricted in turbid habitats (Liu, et al, 2016a).…”

Visual pigment evolution in Characiformes: the dynamic interplay of teleost whole-genome duplication, surviving opsins and spectral tuning

“…Since variation in spectral sensitivities is due, to a large extent, to differences in vitamin A 2 content, it is not surprising that, with the notable exception of G. atracaudatus , there was little variation in blue cone sensitivity across species, as the effects of the chromophore are minimal at short wavelengths (Whitmore and Bowmaker 1989). Chromophore-based spectral tuning is characteristic of fish inhabiting long-wavelength-shifted habitats (Whitmore and Bowmaker 1989; Carleton et al 2006; Toyama et al 2008; Hofmann et al 2009; Miyagi et al 2012; Saarinen et al 2012; Weadick et al 2012; Liu et al 2016; Terai et al 2017; Torres-Dowdall et al 2017; Escobar-Camacho et al 2019), and is well suited to the variable light environments of Neotropical freshwater ecosystems, famously among the most diverse in spectra on the planet, from clear fast-running mountain creeks, to muddy ‘white waters’ (from ‘ agua blanca’ , indicating turbid highly scattering brown-tainted waters), and tannin-rich black waters (Wallace 1865; Costa et al 2013; Escobar-Camacho et al 2019). Finally, non-significant variation in rod chromophore proportions was observed between individuals, with some species exhibiting a similar proportion across individuals, while other species exhibit a larger range (Table S7).…”