Simultaneous Expression of UV and Violet SWS1 Opsins Expands the Visual Palette in a Group of Freshwater Snakes

Abstract

Snakes are known to express a rod visual opsin and two cone opsins, only (SWS1, LWS), a reduced palette resulting from their supposedly fossorial origins. Dipsadid snakes in the genus Helicops are highly visual predators that successfully invaded freshwater habitats from ancestral terrestrial-only habitats. Here we report the first case of multiple SWS1 visual pigments in a vertebrate, simultaneously expressed in different photoreceptors and conferring both UV and violet sensitivity to Helicops snakes. Molecular analysis and in vitro expression confirmed the presence of two functional SWS1 opsins, likely the result of recent gene duplication. Evolutionary analyses indicate that each sws1 variant has undergone different evolutionary paths, with strong purifying selection acting on the UV-sensitive copy and dN/dS ∼1 on the violet-sensitive copy. Site-directed mutagenesis points to the functional role of a single amino acid substitution, Phe86Val, in the large spectral shift between UV and violet opsins. In addition, higher densities of photoreceptors and SWS1 cones in the ventral retina suggest improved acuity in the upper visual field possibly correlated with visually-guided behaviors. The expanded visual opsin repertoire and specialized retinal architecture are likely to improve photon uptake in underwater and terrestrial environments, and provide the neural substrate for a gain in chromatic discrimination, potentially conferring unique color vision in the UV-violet range. Our findings highlight the innovative solutions undertaken by a highly specialized lineage to tackle the challenges imposed by the invasion of novel photic environments and the extraordinary diversity of evolutionary trajectories taken by visual opsin-based perception in vertebrates.

Functional Duplication of the Short-Wavelength-Sensitive Opsin in Sea Snakes: Evidence for Reexpanded Color Sensitivity Following Ancestral Regression

“…Old World primates and Howler monkeys gained trichromacy by duplication and divergence of the LWS opsin ( Jacobs et al 1996 ; Hunt et al 1998 ; Dulai et al 1999 ), and females of many New World primate lineages gained a similar trichromacy via allelic polymorphism of the X-linked LWS opsin ( Carvalho et al 2017 ). The two spectrally distinct SWS1 opsins observed in semiaquatic Helicops snakes are likely the result of a recent gene duplication ( Hauzman et al 2021 ) and, before our study, represent the only report of SWS1 duplication in a tetrapod. This imbalance between opsin losses versus gains in tetrapods leaves open the question of whether functional duplication commonly compensates for ancestral gene losses in visual and other sensory systems underpinned by multigene receptor families.…”

Diversity and Evolution of Frog Visual Opsins: Spectral Tuning and Adaptation to Distinct Light Environments

“…Opsin gene duplication in tetrapods is rare and most known instances have occurred in nontetrapods (specifically teleost fishes; Musilova et al 2021 ). In tetrapods, known duplications are restricted to mammals (some marsupials and primates; Cowing et al 2008 ; Carvalho et al 2017 ), snakes ( Hauzman et al 2021 ; Rossetto et al 2023 ), and frogs ( Feehan et al 2017 ; Schott et al 2022b ). Several frog species are polyploids, and thus may have more than one functional copy of each opsin gene, although often one of the homologs is lost.…”

Dynamic Expansions and Retinal Expression of Spectrally Distinct Short-Wavelength Opsin Genes in Sea Snakes

“…In particular, teleost fish have undergone extensive expansions in multiple independent lineages (Musilova et al 2021), resulting in complements of up to 38 intact visual opsins (Musilova et al 2019). Tetrapods, in contrast, are so far known to have undergone only four functional expansions, with the addition of between one and three or four intact genes in each lineage (Jacobs et al 1996;Hunt et al 1998;Dulai et al 1999;Hauzman et al 2021;Rossetto et al 2023). The primary drivers of variation in gene copy number are structural genomic architecture (Chen et al 2014), which underpins propensity for duplication events, and ecological selection pressures, which determine the persistence of genes within populations.…”

“…The duplications of MWS/LWS in primate lineages are suspected to have occurred by unequal crossing over of sister chromatids during recombination (Nathans et al 1986;Hunt et al 1998), sometimes promoted by Alu transposons (Dulai et al 1999). Whole-genome duplications have not been reported in reptiles (Otto & Whitton 2000;Mable 2004) and visual opsin duplication has been described in only two lineages (Hauzman et al 2021;Rossetto et al 2023).…”

“…Interestingly, both of the currently known visual opsin expansions in reptiles have occurred in the SWS1 of aquatic snakes (Hauzman et al 2021;Rossetto et al 2023). Most snakes possess only two cone-expressed visual opsins (SWS1 and LWS) following a dim-light bottleneck which resulted in losses of SWS2 and RH2 in their earliest ancestors (Simões et al 2015).…”