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. Molecul… Show more
“…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.…”
Color vision is mediated by ancient and spectrally distinct cone opsins. Yet, while there have been multiple losses of opsin genes during the evolution of tetrapods, evidence for opsin gains via functional duplication is extremely scarce. Previous studies have shown that some secondarily marine elapid snakes have acquired expanded “UV–blue” sensitivity via changes at key spectral tuning amino acid sites of the Short-Wavelength Opsin 1 (SWS1) gene. Here, we use elapid reference genomes to show that the molecular origin of this adaptation involved repeated, proximal duplications of the SWS1 gene in the fully marine Hydrophis cyanocinctus. This species possesses four intact SWS1 genes; two of these genes have the ancestral UV sensitivity, and two have a derived sensitivity to the longer wavelengths that dominate marine habitats. We suggest that this remarkable expansion of the opsin repertoire of sea snakes functionally compensates for the ancestral losses of two middle-wavelength opsins in the earliest (dim-light adapted) snakes. This provides a striking contrast to the evolution of opsins during ecological transitions in mammals. Like snakes, early mammals lost two cone photopigments; however, lineages such as bats and cetaceans underwent further opsin losses during their adaptation to dim-light environments.
“…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.…”
Color vision is mediated by ancient and spectrally distinct cone opsins. Yet, while there have been multiple losses of opsin genes during the evolution of tetrapods, evidence for opsin gains via functional duplication is extremely scarce. Previous studies have shown that some secondarily marine elapid snakes have acquired expanded “UV–blue” sensitivity via changes at key spectral tuning amino acid sites of the Short-Wavelength Opsin 1 (SWS1) gene. Here, we use elapid reference genomes to show that the molecular origin of this adaptation involved repeated, proximal duplications of the SWS1 gene in the fully marine Hydrophis cyanocinctus. This species possesses four intact SWS1 genes; two of these genes have the ancestral UV sensitivity, and two have a derived sensitivity to the longer wavelengths that dominate marine habitats. We suggest that this remarkable expansion of the opsin repertoire of sea snakes functionally compensates for the ancestral losses of two middle-wavelength opsins in the earliest (dim-light adapted) snakes. This provides a striking contrast to the evolution of opsins during ecological transitions in mammals. Like snakes, early mammals lost two cone photopigments; however, lineages such as bats and cetaceans underwent further opsin losses during their adaptation to dim-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.…”
Visual systems adapt to different light environments through several avenues including optical changes to the eye and neurological changes in how light signals are processed and interpreted. Spectral sensitivity can evolve via changes to visual pigments housed in the retinal photoreceptors through gene duplication and loss, differential and coexpression, and sequence evolution. Frogs provide an excellent, yet understudied, system for visual evolution research due to their diversity of ecologies (including biphasic aquatic-terrestrial life cycles) that we hypothesize imposed different selective pressures leading to adaptive evolution of the visual system, notably the opsins that encode the protein component of the visual pigments responsible for the first step in visual perception. Here, we analyze the diversity and evolution of visual opsin genes from 93 new eye transcriptomes plus published data for a combined dataset spanning 122 frog species and 34 families. We find that most species express the four visual opsins previously identified in frogs but show evidence for gene loss in two lineages. Further, we present evidence of positive selection in three opsins and shifts in selective pressures associated with differences in habitat and life history, but not activity pattern. We identify substantial novel variation in the visual opsins and, using microspectrophotometry, find highly variable spectral sensitivities, expanding known ranges for all frog visual pigments. Mutations at spectral-tuning sites only partially account for this variation, suggesting that frogs have used tuning pathways that are unique among vertebrates. These results support the hypothesis of adaptive evolution in photoreceptor physiology across the frog tree of life in response to varying environmental and ecological factors and further our growing understanding of vertebrate visual evolution.
“…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.…”
Section: Introductionmentioning
confidence: 99%
“…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).…”
Section: Introductionmentioning
confidence: 99%
“…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).…”
The photopigment-encoding visual opsin genes that mediate colour perception show great variation in copy number and adaptive function across vertebrates. An open question is how this variation has been shaped by the interaction of lineage-specific structural genomic architecture and ecological selection pressures. We contribute to this issue by investigating the expansion dynamics and expression of the duplicated Short-Wavelength-Sensitive-1 opsin (SWS1) in sea snakes (Elapidae). We generated one new genome, 45 resequencing datasets, 10 retinal transcriptomes, and 81 SWS1 exon sequences for sea snakes, and analysed these alongside 16 existing genomes for sea snakes and their terrestrial relatives. Our analyses revealed multiple independent transitions in SWS1 copy number in the marineHydrophisclade, with at least three lineages having multiple intact SWS1 genes: the previously studiedHydrophis cyanocinctusand at least two close relatives of this species;H. atriceps-H. fasciatus;and an individualH. curtus. In each lineage, gene copy divergence at a key spectral tuning site resulted in distinct UV and Violet/Blue-sensitive SWS1 subtypes. Both spectral variants were simultaneously expressed in the retinae ofH. cyanocinctusandH. atriceps,providing the first evidence that these SWS1 expansions confer novel phenotypes. Finally, chromosome annotation for nine species revealed shared structural features in proximity to SWS1 regardless of copy number. If these features are associated with SWS1 duplication, expanded opsin complements could be more common in snakes than is currently recognised. Alternatively, selection pressures specific to aquatic environments could favour improved chromatic distinction in just some lineages.SignificanceSecondary transitions to marine environments are commonly accompanied by pseudogenisation of the visual opsin genes which mediate colour perception. Conversely, a species of fully-marine hydrophiid snake has functionally expanded its short-wavelength-sensitive opsin repertoire following a terrestrial ancestry. The current study explores this further by mapping opsin copy number across the hydrophiid phylogeny and by quantifying expression of SWS1 subtypes within sea snake retinae. Despite few reports of opsin expansions in tetrapods, we provide evidence for the occurrence of multiple expansion events throughoutHydrophis. Most intriguingly, retinal expression of spectrally-divergent copies implies a functionally-significant phenotype; possibly even trichromacy.
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