Evolution and spectral tuning of visual pigments in birds and mammals

Variation in the types and spectral characteristics of visual pigments is a common mechanism for the adaptation of the vertebrate visual system to prevailing light conditions. The extent of this diversity in mammals and birds is discussed in detail in this review, alongside an in-depth consideration of the molecular changes involved. In mammals, a nocturnal stage in early evolution is thought to underlie the reduction in the number of classes of cone visual pigment genes from four to only two, with the secondary loss of one of these genes in many monochromatic nocturnal and marine species. The trichromacy seen in many primates arises from either a polymorphism or duplication of one of these genes. In contrast, birds have retained the four ancestral cone visual pigment genes, with a generally conserved expression in either single or double cone classes. The loss of sensitivity to ultraviolet (UV) irradiation is a feature of both mammalian and avian visual evolution, with UV sensitivity retained among mammals by only a subset of rodents and marsupials. Where it is found in birds, it is not ancestral but newly acquired.

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The spectral transmission of ocular media suggests ultraviolet sensitivity is widespread among mammals

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2013.2995 ◽

2014 ◽

Vol 281 (1780) ◽

pp. 20132995 ◽

Cited By ~ 61

Author(s):

R. H. Douglas ◽

G. Jeffery

Keyword(s):

Energy Level ◽

Visual Pigment ◽

High Spatial Resolution ◽

Mammalian Species ◽

Visual Pigments ◽

Spectral Transmission ◽

Tree Shrews ◽

Uv Sensitivity ◽

Ultraviolet Sensitivity ◽

Ocular Media

Although ultraviolet (UV) sensitivity is widespread among animals it is considered rare in mammals, being restricted to the few species that have a visual pigment maximally sensitive ( λ max ) below 400 nm. However, even animals without such a pigment will be UV-sensitive if they have ocular media that transmit these wavelengths, as all visual pigments absorb significant amounts of UV if the energy level is sufficient. Although it is known that lenses of diurnal sciurid rodents, tree shrews and primates prevent UV from reaching the retina, the degree of UV transmission by ocular media of most other mammals without a visual pigment with λ max in the UV is unknown. We examined lenses of 38 mammalian species from 25 families in nine orders and observed large diversity in the degree of short-wavelength transmission. All species whose lenses removed short wavelengths had retinae specialized for high spatial resolution and relatively high cone numbers, suggesting that UV removal is primarily linked to increased acuity. Other mammals, however, such as hedgehogs, dogs, cats, ferrets and okapis had lenses transmitting significant amounts of UVA (315–400 nm), suggesting that they will be UV-sensitive even without a specific UV visual pigment.

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Visual pigments in a palaeognath bird, the emu Dromaius novaehollandiae : implications for spectral sensitivity and the origin of ultraviolet vision

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2016.1063 ◽

2016 ◽

Vol 283 (1834) ◽

pp. 20161063 ◽

Cited By ~ 8

Author(s):

Nathan S. Hart ◽

Jessica K. Mountford ◽

Wayne I. L. Davies ◽

Shaun P. Collin ◽

David M. Hunt

Keyword(s):

Spectral Sensitivity ◽

Visual Pigment ◽

Spectral Characteristics ◽

Bird Species ◽

Visual Pigments ◽

Ancestral State ◽

Avian Evolution ◽

Retinal Photoreceptors ◽

Cone Type ◽

Dromaius Novaehollandiae

A comprehensive description of the spectral characteristics of retinal photoreceptors in palaeognaths is lacking. Moreover, controversy exists with respect to the spectral sensitivity of the short-wavelength-sensitive-1 (SWS1) opsin-based visual pigment expressed in one type of single cone: previous microspectrophotometric (MSP) measurements in the ostrich ( Struthio camelus ) suggested a violet-sensitive (VS) SWS1 pigment, but all palaeognath SWS1 opsin sequences obtained to date (including the ostrich) imply that the visual pigment is ultraviolet-sensitive (UVS). In this study, MSP was used to measure the spectral properties of visual pigments and oil droplets in the retinal photoreceptors of the emu ( Dromaius novaehollandiae ). Results show that the emu resembles most other bird species in possessing four spectrally distinct single cones, as well as double cones and rods. Four cone and a single rod opsin are expressed, each an orthologue of a previously identified pigment. The SWS1 pigment is clearly UVS (wavelength of maximum absorbance [ λ max ] = 376 nm), with key tuning sites (Phe86 and Cys90) consistent with other vertebrate UVS SWS1 pigments. Palaeognaths would appear, therefore, to have UVS SWS1 pigments. As they are considered to be basal in avian evolution, this suggests that UVS is the most likely ancestral state for birds. The functional significance of a dedicated UVS cone type in the emu is discussed.

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Ultraviolet vision in larval Neogonodactylus oerstedii

Journal of Experimental Biology ◽

10.1242/jeb.243256 ◽

2022 ◽

Author(s):

Marisa S. McDonald ◽

Sitara Palecanda ◽

Jonathan H. Cohen ◽

Megan L. Porter

Keyword(s):

Visual Pigment ◽

Molecular Diversity ◽

Animal Kingdom ◽

Uv Sensitivity ◽

Color Detection ◽

Uv Vision ◽

Ultraviolet Vision ◽

The Caribbean ◽

Different Color ◽

Spectral Channels

Stomatopod crustaceans have among the most complex eyes in the animal kingdom, with up to twelve different color detection channels. The capabilities of these unique eyes include photoreception of ultraviolet (UV) wavelengths (<400 nm). UV vision has been well characterized in adult stomatopods but has not been previously demonstrated in the comparatively simpler larval eye. Larval stomatopod eyes are developmentally distinct from their adult counterpart and have been described as lacking the visual pigment diversity and morphological specializations found in adult eyes. However, recent studies have provided evidence that larval stomatopod eyes are more complex than previously thought and warrant closer investigation. Using electroretinogram recordings in live animals we found physiological evidence of blue and UV sensitive photoreceptors in larvae of the Caribbean stomatopod species Neogonodactylus oerstedii. Transcriptomes of individual larvae were used to identify the expression of three distinct UV opsins transcripts, which may indicate the presence of multiple UV spectral channels. This is the first paper to document UV vision in any larval stomatopod, expanding our understanding of the importance of UV sensitivity in plankton. Similar to adults, larval stomatopod eyes are more complex than expected and contain previously uncharacterized molecular diversity and physiological functions.

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Spectral absorbance, structure, and population density of photoreceptors in the retina of the lake sturgeon (Acipenser fulvescens)

Canadian Journal of Zoology ◽

10.1139/z07-033 ◽

2007 ◽

Vol 85 (4) ◽

pp. 584-587 ◽

Cited By ~ 4

Author(s):

A.J. Sillman ◽

E.K. Ong ◽

E.R. Loew

Keyword(s):

Visual Pigment ◽

Visual Pigments ◽

Lake Sturgeon ◽

Acipenser Fulvescens ◽

Long Wavelength ◽

Rods And Cones ◽

The North ◽

Spectral Absorbance ◽

Dim Light ◽

Scanning Electron

Lake sturgeon ( Acipenser fulvescens Rafinesque, 1817) photoreceptors were studied with scanning electron microscopy and microspectrophotometry. The retina contains both rods and cones, with cones estimated composing about 30% of the photoreceptor population. Only large single cones were identified and they are similar to those found in other species of the order Acipenseriformes. The rods are large, with long, broad outer segments, and are similar to the dominant rod found in other sturgeons and the North American paddlefish ( Polyodon spathula (Walbaum, 1792)). Mean (SD) rod packing density at 22 624 ± 3 509 rods/mm2 is low compared with those of other animals that function primarily in dim light. The visual pigment of the rods has a mean (SD) peak absorbance (λmax) at 541 ± 2 nm. Three different cone populations were identified: a long wavelength sensitive cone containing a visual pigment with λmax at 619 ± 3 nm; middle wavelength sensitive cone with λmax at 538 ± 1 nm; and short wavelength sensitive cone with λmax at 448 ± 1 nm. All the visual pigments are based on the vitamin A2 chromophore.

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A locus control region adjacent to the human red and green visual pigment genes

Neuron ◽

10.1016/0896-6273(92)90181-c ◽

1992 ◽

Vol 9 (3) ◽

pp. 429-440 ◽

Cited By ~ 250

Author(s):

Yanshu Wang ◽

Jennifer P. Macke ◽

Shannath L. Merbs ◽

Donald J. Zack ◽

Brenda Klaunberg ◽

...

Keyword(s):

Control Region ◽

Visual Pigment ◽

Locus Control Region ◽

Pigment Genes

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The photoreceptors and visual pigments in the retina of the white sturgeon, Acipenser transmontanus

Canadian Journal of Zoology ◽

10.1139/z90-228 ◽

1990 ◽

Vol 68 (7) ◽

pp. 1544-1551 ◽

Cited By ~ 28

Author(s):

A. J. Sillman ◽

M. D. Spanfelner ◽

E. R. Loew

Keyword(s):

Vitamin A ◽

Visual Pigment ◽

Visual Pigments ◽

Spectrophotometric Analysis ◽

White Sturgeon ◽

Acipenser Transmontanus ◽

Light Regimen ◽

Cone Pigment ◽

Spectral Absorbance

The photoreceptors in the retina of the white sturgeon, Acipenser transmontanus (Chondrostei), were studied by means of scanning electron microscopy, in situ microspectrophotometry, and spectrophotometric analysis of visual pigment extracts. The white sturgeon retina is simple in that it contains only two morphologically distinct photoreceptors. The retina is dominated by rods with large outer segments, but there is a substantial population (40%) of single cones. Evidence was found for only one rod visual pigment and one cone visual pigment. Peak spectral absorbance (λmax) of the rod pigment is near 539 nm, whereas λmax of the cone pigment is near 605 nm. Both visual pigments are porphyropsin types with chromophores based on vitamin A2. No detectable rhodopsin based on vitamin A1 is ever present, regardless of season or light regimen. The results are discussed in terms of the sturgeon's behavior, as well as the implications for the evolution of color vision.

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Visual pigments and oil droplets in diurnal lizards

Journal of Experimental Biology ◽

10.1242/jeb.205.7.927 ◽

2002 ◽

Vol 205 (7) ◽

pp. 927-938 ◽

Cited By ~ 9

Author(s):

Ellis R. Loew ◽

Leo J. Fleishman ◽

Russell G. Foster ◽

Ignacio Provencio

Keyword(s):

Visual Pigment ◽

Visual Pigments ◽

Anolis Carolinensis ◽

Visual Cell ◽

Oil Droplets ◽

Oil Droplet ◽

Long Wavelength ◽

Apparent Color ◽

Vitamin A2 ◽

Insight Into

SUMMARY We report microspectrophotometric (MSP) data for the visual pigments and oil droplets of 17 species of Caribbean anoline lizard known to live in differing photic habitats and having distinctly different dewlap colors. The outgroup Polychrus marmoratus was also examined to gain insight into the ancestral condition. Except for Anolis carolinensis, which is known to use vitamin A2 as its visual pigment chromophore, all anoline species examined possessed at least four vitamin-A1-based visual pigments with maximum absorbance (λmax) at 564, 495,455 and 365 nm. To the previously reported visual pigments for A. carolinensis we add an ultraviolet-sensitive one withλ max at 365 nm. Five common classes of oil droplet were measured, named according to apparent color and associated with specific cone classes — yellow and green in long-wavelength-sensitive (LWS) cones,green only in medium-wavelength-sensitive (MWS) cones and colorless in short-wavelength-sensitive (SWS) and ultraviolet-sensitive (UVS) cones. MSP data showed that the colorless droplet in the SWS cone had significant absorption between 350 and 400 nm, while the colorless droplet in the UVS cone did not. The pattern for Polychrus marmoratus was identical to that for the anoles except for the presence of a previously undescribed visual cell with a rod-like outer segment, a visual pigment with a λmaxof 497 nm and a colorless oil droplet like that in the UVS cones. These findings suggest that anoline visual pigments, as far as they determine visual system spectral sensitivity, are not necessarily adapted to the photic environment or to the color of significant visual targets (e.g. dewlaps).

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Visual pigments, oil droplets and cone photoreceptor distribution in the european starling (Sturnus vulgaris)

Journal of Experimental Biology ◽

10.1242/jeb.201.9.1433 ◽

1998 ◽

Vol 201 (9) ◽

pp. 1433-1446 ◽

Cited By ~ 11

Author(s):

N S Hart ◽

J C Partridge ◽

I C Cuthill

Keyword(s):

Visual Pigment ◽

Sturnus Vulgaris ◽

European Starling ◽

Visual Pigments ◽

Double Cone ◽

Temporal Region ◽

Oil Droplets ◽

Tetrazolium Chloride ◽

Oil Droplet ◽

Single Cone

Microspectrophotometric measurements of retinal photoreceptors from the European starling (Sturnus vulgaris) revealed four classes of single cone, containing visual pigments with wavelengths of maximum absorbance (<IMG src="/images/symbols/lambda.gif" WIDTH="8" HEIGHT="12" ALIGN="BOTTOM" NATURALSIZEFLAG= "3">max) at 563, 504, 449 and close to 362 nm. The two longer-wave-sensitive single cones contained brightly coloured oil droplets which cut off light below 572 and 514 nm, respectively. The 449 nm <IMG src="/images/symbols/lambda.gif" WIDTH="8" HEIGHT="12" ALIGN="BOTTOM" NATURALSIZEFLAG="3">max pigment was associated with a 'colourless' oil droplet with peak measured absorptance below 400 nm. The ultraviolet-sensitive visual pigment was paired with a transparent oil droplet which showed no significant absorption above 350 nm. A single class of double cone was identified, both members of which contained the longwave-sensitive (<IMG src="/images/symbols/lambda.gif" WIDTH="8" HEIGHT= "12" ALIGN="BOTTOM" NATURALSIZEFLAG="3">max 563 nm) visual pigment. The principal member of the double cone contained an oil droplet with a topographically variable cut-off wavelength below 471 nm; the oil droplet found in the accessory member was only measured in the ventral retina and displayed three distinct peaks of absorption at approximately 430, 450 and 480 nm. Rod photoreceptors had a <IMG src="/images/symbols/lambda.gif" WIDTH="8" HEIGHT="12" ALIGN="BOTTOM" NATURALSIZEFLAG="3">max at 503 nm. A new polynomial for fitting visual pigment templates to ultraviolet-sensitive visual pigment data is given. Topographic density measurements of the different cone classes were made using Nitroblue-tetrazolium chloride to label selectively bleached photoreceptors. The two classes of shortwave-sensitive single cone were more abundant in the dorsal retina, and longwave-sensitive single cones were notably less abundant in the dorso-temporal region of the retina, which subserves binocular vision.

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