Functional preservation and variation in the cone opsin genes of nocturnal tarsiers

The short-wavelength sensitive (S-) opsin gene OPN1SW is pseudogenized in some nocturnal primates and retained in others, enabling dichromatic colour vision. Debate on the functional significance of this variation has focused on dark conditions, yet many nocturnal species initiate activity under dim (mesopic) light levels that can support colour vision. Tarsiers are nocturnal, twilight-active primates and exemplary visual predators; they also express different colour vision phenotypes, raising the possibility of discrete adaptations to mesopic conditions. To explore this premise, we conducted a field study in two stages. First, to estimate the level of functional constraint on colour vision, we sequenced OPN1SW in 12 wild-caught Philippine tarsiers ( Tarsius syrichta ). Second, to explore whether the dichromatic visual systems of Philippine and Bornean ( Tarsius bancanus ) tarsiers—which express alternate versions of the medium/long-wavelength sensitive (M/L-) opsin gene OPN1MW / OPN1LW —confer differential advantages specific to their respective habitats, we used twilight and moonlight conditions to model the visual contrasts of invertebrate prey. We detected a signature of purifying selection for OPN1SW , indicating that colour vision confers an adaptive advantage to tarsiers. However, this advantage extends to a relatively small proportion of prey–background contrasts, and mostly brown arthropod prey amid leaf litter. We also found that the colour vision of T. bancanus is advantageous for discriminating prey under twilight that is enriched in shorter (bluer) wavelengths, a plausible idiosyncrasy of understorey habitats in Borneo. This article is part of the themed issue ‘Vision in dim light’.

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Opsin gene repertoires in northern archaic hominids

Genome ◽

10.1139/gen-2015-0164 ◽

2016 ◽

Vol 59 (8) ◽

pp. 541-549 ◽

Cited By ~ 1

Author(s):

John S. Taylor ◽

Thomas E. Reimchen

Keyword(s):

Colour Vision ◽

Modern Human ◽

Active Species ◽

Opsin Gene ◽

Human Reference Genome ◽

Northern Latitudes ◽

Opsin Genes ◽

Northern Distribution ◽

Dim Light ◽

Additional Support

The Neanderthals’ northern distribution, hunting techniques, and orbit breadths suggest that they were more active in dim light than modern humans. We surveyed visual opsin genes from four Neanderthals and two other archaic hominids to see if they provided additional support for this hypothesis. This analysis was motivated by the observation that alleles responsible for anomalous trichromacy in humans are more common in northern latitudes, by data suggesting that these variants might enhance vision in mesopic conditions, and by the observation that dim light active species often have fewer opsin genes than diurnal relatives. We also looked for evidence of convergent amino acid substitutions in Neanderthal opsins and orthologs from crepuscular or nocturnal species. The Altai Neanderthal, the Denisovan, and the Ust’-Ishim early modern human had opsin genes that encoded proteins identical to orthologs in the human reference genome. Opsins from the Vindija Cave Neanderthals (three females) had many nonsynonymous substitutions, including several predicted to influence colour vision (e.g., stop codons). However, the functional implications of these observations were difficult to assess, given that “control” loci, where no substitutions were expected, differed from humans to the same extent. This left unresolved the test for colour vision deficiencies in Vindija Cave Neanderthals.

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Opsin genes of select treeshrews resolve ancestral character states within Scandentia

Royal Society Open Science ◽

10.1098/rsos.182037 ◽

2019 ◽

Vol 6 (4) ◽

pp. 182037

Author(s):

Gwen Duytschaever ◽

Mareike C. Janiak ◽

Perry S. Ong ◽

Konstans Wells ◽

Nathaniel J. Dominy ◽

...

Keyword(s):

Purifying Selection ◽

Opsin Gene ◽

Functional Variation ◽

Long Wavelength ◽

Living Fossils ◽

Opsin Genes ◽

Senior Synonym ◽

Peak Sensitivity ◽

Encoding Genes ◽

Ancestral Character States

Treeshrews are small, squirrel-like mammals in the order Scandentia, which is nested together with Primates and Dermoptera in the superordinal group Euarchonta. They are often described as living fossils, and researchers have long turned to treeshrews as a model or ecological analogue for ancestral primates. A comparative study of colour vision-encoding genes within Scandentia found a derived amino acid substitution in the long-wavelength sensitive opsin gene ( OPN1LW ) of the Bornean smooth-tailed treeshrew ( Dendrogale melanura ). The opsin, by inference, is red-shifted by ca 6 nm with an inferred peak sensitivity of 561 nm. It is tempting to view this trait as a novel visual adaptation; however, the genetic and functional diversity of visual pigments in treeshrews is unresolved outside of Borneo. Here, we report gene sequences from the northern smooth-tailed treeshrew ( Dendrogale murina ) and the Mindanao treeshrew ( Tupaia everetti , the senior synonym of Urogale everetti ). We found that the opsin genes are under purifying selection and that D. murina shares the same substitution as its congener, a result that distinguishes Dendrogale from other treeshrews, including T. everetti. We discuss the implications of opsin functional variation in light of limited knowledge about the visual ecology of smooth-tailed treeshrews.

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Uniform trichromacy in Alouatta caraya and Alouatta seniculus: behavioural and genetic colour vision evaluation

Frontiers in Zoology ◽

10.1186/s12983-021-00421-0 ◽

2021 ◽

Vol 18 (1) ◽

Author(s):

Leonardo Dutra Henriques ◽

Einat Hauzman ◽

Daniela Maria Oliveira Bonci ◽

Belinda S. W. Chang ◽

José Augusto Pereira Carneiro Muniz ◽

...

Keyword(s):

Genetic Analysis ◽

Colour Vision ◽

Opsin Gene ◽

Alouatta Seniculus ◽

Colour Discrimination ◽

Discrimination Capability ◽

Cone Opsin ◽

Behavioural Test ◽

532 Nm ◽

Active Genes

AbstractPrimate colour vision depends on a matrix of photoreceptors, a neuronal post receptoral structure and a combination of genes that culminate in different sensitivity through the visual spectrum. Along with a common cone opsin gene for short wavelengths (sws1), Neotropical primates (Platyrrhini) have only one cone opsin gene for medium-long wavelengths (mws/lws) per X chromosome while Paleotropical primates (Catarrhini), including humans, have two active genes. Therefore, while female platyrrhines may be trichromats, males are always dichromats. The genus Alouatta is inferred to be an exception to this rule, as electrophysiological, behavioural and molecular analyses indicated a potential for male trichromacy in this genus. However, it is very important to ascertain by a combination of genetic and behavioural analyses whether this potential translates in terms of colour discrimination capability. We evaluated two howler monkeys (Alouatta spp.), one male A. caraya and one female A. seniculus, using a combination of genetic analysis of the opsin gene sequences and a behavioral colour discrimination test not previously used in this genus. Both individuals completed the behavioural test with performances typical of trichromatic colour vision and the genetic analysis of the sws1, mws, and lws opsin genes revealed three different opsin sequences in both subjects. These results are consistent with uniform trichromacy in both male and female, with presumed spectral sensitivity peaks similar to Catarrhini, at ~ 430 nm, 532 nm, and 563 nm for S-, M- and L-cones, respectively.

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Rod and cone function in coneless mice

Visual Neuroscience ◽

10.1017/s095252380522610x ◽

2005 ◽

Vol 22 (6) ◽

pp. 807-816 ◽

Cited By ~ 7

Author(s):

GARY A. WILLIAMS ◽

KRISTIN A. DAIGLE ◽

GERALD H. JACOBS

Keyword(s):

Opsin Gene ◽

Wild Type ◽

Normal Complement ◽

Cone Opsin ◽

Light Levels ◽

Age Related ◽

Rod System ◽

Cone Function ◽

Flicker Erg ◽

Flanking Sequences

Transgenic coneless mice were initially developed to study retinal function in the absence of cones. In coneless mice created by expressing an attenuated diphtheria toxin under the control of flanking sequences from the human L-cone opsin gene, a small number of cones (3–5% of the normal complement) survive in a retina that otherwise appears structurally quite normal. These cones predominantly (∼87% of the total) contain UV-sensitive photopigment. ERG recordings, photoreceptor labeling, and behavioral measurements were conducted on coneless and wild-type mice to better understand how the nature of this alteration in receptor complement impacts vision. Signals from the small residual population of UV cones are readily detected in the flicker ERG where they yield signal amplitudes at saturation that are roughly proportional to the number of surviving cones. Behavioral measurements show that rod-based vision in coneless mice does not differ significantly from that of wild-type mice, nor does their rod system show any evidence of age-related deterioration. Coneless mice are able to make accurate rod-based visual discriminations at light levels well in excess of those required to reach cone threshold in wild-type mice.

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X-linked cone dystrophy and colour vision deficiency arising from a missense mutation in a hybrid L/M cone opsin gene

Vision Research ◽

10.1016/j.visres.2012.12.012 ◽

2013 ◽

Vol 80 ◽

pp. 41-50 ◽

Cited By ~ 9

Author(s):

Michelle McClements ◽

Wayne I.L. Davies ◽

Michel Michaelides ◽

Joseph Carroll ◽

Jungtae Rha ◽

...

Keyword(s):

Missense Mutation ◽

Colour Vision ◽

Opsin Gene ◽

Cone Dystrophy ◽

Cone Opsin ◽

Colour Vision Deficiency

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

Brain Behavior and Evolution ◽

10.1159/000450746 ◽

2016 ◽

Vol 88 (3-4) ◽

pp. 204-212 ◽

Cited By ~ 6

Author(s):

Da-Wei Liu ◽

Ying Lu ◽

Hong Young Yan ◽

Harold H. Zakon

Keyword(s):

Short Wavelength ◽

Electric Fish ◽

Sister Group ◽

Weakly Electric Fish ◽

Opsin Gene ◽

South American ◽

Long Wavelength ◽

Cone Opsin ◽

Opsin Genes ◽

Weakly Electric

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.

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Evidence for UV-green dichromacy in the basal hymenopteran Sirex noctilio (Siricidae)

Scientific Reports ◽

10.1038/s41598-021-95107-2 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Quentin Guignard ◽

Johannes Spaethe ◽

Bernard Slippers ◽

Martin Strube-Bloss ◽

Jeremy D. Allison

Keyword(s):

Colour Vision ◽

Compound Eye ◽

Phylogenetic Analyses ◽

Ultra Violet ◽

Opsin Gene ◽

Compound Eyes ◽

Sirex Noctilio ◽

Long Wavelength ◽

Opsin Genes ◽

Related Group

AbstractA precondition for colour vision is the presence of at least two spectral types of photoreceptors in the eye. The order Hymenoptera is traditionally divided into the Apocrita (ants, bees, wasps) and the Symphyta (sawflies, woodwasps, horntails). Most apocritan species possess three different photoreceptor types. In contrast, physiological studies in the Symphyta have reported one to four photoreceptor types. To better understand the evolution of photoreceptor diversity in the Hymenoptera, we studied the Symphyta Sirex noctilio, which belongs to the superfamily Siricoidea, a closely related group of the Apocrita suborder. Our aim was to (i) identify the photoreceptor types of the compound eye by electroretinography (ERG), (ii) characterise the visual opsin genes of S. noctilio by genomic comparisons and phylogenetic analyses and (iii) analyse opsin mRNA expression. ERG measurements revealed two photoreceptor types in the compound eye, maximally sensitive to 527 and 364 nm. In addition, we identified three opsins in the genome, homologous to the hymenopteran green or long-wavelength sensitive (LW) LW1, LW2 and ultra-violet sensitive (UV) opsin genes. The LW1 and UV opsins were found to be expressed in the compound eyes, and LW2 and UV opsins in the ocelli. The lack of a blue or short-wavelength sensitive (SW) homologous opsin gene and a corresponding receptor suggests that S. noctilio is a UV-green dichromate.

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Multiple ancestral duplications of the red-sensitive opsin gene (LWS) in teleost fishes and convergent spectral shifts to green vision in gobies

10.1101/2021.05.08.443214 ◽

2021 ◽

Author(s):

Fabio Cortesi ◽

Daniel Escobar Camacho ◽

Martin Luehrmann ◽

Gina Maria Sommer ◽

Zuzana Musilova

Keyword(s):

Genome Duplication ◽

In Situ Hybridisation ◽

Bright Light ◽

Opsin Gene ◽

Colour Perception ◽

Long Wavelength ◽

Cone Opsin ◽

Spectral Shifts ◽

Functional Replacement

Photopigments, consisting of an opsin protein bound to a light-sensitive chromophore, are at the centre of vertebrate vision. The vertebrate ancestor already possessed four cone opsin classes involved in colour perception during bright-light conditions, which are sensitive from the ultraviolet to the red-wavelengths of light. Teleosts experienced an extra round of whole genome duplication (3R) at their origin, and while most teleosts maintained only one long-wavelength-sensitive opsin gene (LWS1), the second ancestral copy (LWS2) persisted in characins and osteoglossomorphs. Following 3R, teleost opsins have continued to expand and diversify, which is thought to be a consequence of the different light environment fishes inhabit, from clear streams to the relative darkness of the deep-sea. Although many recent and a few ancestral opsin duplicates can be found, none predating the 3R were thought to exist. In this study we report on a second, previously unnoticed ancestral duplication of the red-sensitive opsin (LWS3), which predates the teleost-specific genome duplication and only persists in gobiid fishes. This is surprising, since it implies that LWS3 has been lost at least 19-20 times independently along the teleost phylogeny. Mining 109 teleost genomes we also uncover a third lineage, the elopomorphs, that maintained the LWS2 copy. We identify convergent amino acid changes that green-shift ancestral and recent LWS copies, leading to adaptive differentiation and the functional replacement of the original green-sensitive RH2 opsin. Retinal transcriptomes and in-situ hybridisation show that LWS3 is expressed to various extents in gobies and in the case of the whitebarred goby, Amblygobius phalaena, it occurs in a separate photoreceptor to LWS1. Our study highlights the importance of comparative studies to comprehend evolution of gene function.

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Birds in the Dark: Complementary and Partial Information

10.1093/oso/9780199694532.003.0006 ◽

2017 ◽

Author(s):

Graham R. Martin

Keyword(s):

Annual Cycle ◽

Colour Vision ◽

Partial Information ◽

Night Time ◽

Light Levels ◽

Night Feeding ◽

Nocturnal Species ◽

Length Changes

Night-time poses exacting problems for vision, resolution inevitably falls and colour vision is not possible as light levels decrease to those of natural night time. Furthermore, light levels are highly variable depending upon whether there is moonlight, and night length changes dramatically in the annual cycle according to latitude. Few birds exploit the resources available at night. Those that do rely upon information received from vision complemented by information from other senses (hearing, olfaction, and touch), and upon highly specialized and restricted behaviours. However, many birds occasionally exploit night-time, e.g. during migration, arriving and departing from nests, and occasional night feeding. Some seabirds dive to such depths that they experience night-time light levels when foraging. Truly nocturnal species such as owls, kiwi, and oilbirds are highly sedentary, and this is essential to allow them to interpret correctly the partial information that is available to them.

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