Losses of functional opsin genes, short-wavelength cone photopigments, and color vision--a significant trend in the evolution of mammalian vision.

All mammalian cone photopigments are derived from the operation of representatives from two opsin gene families (SWS1 and LWS in marsupial and eutherian mammals; SWS2 and LWS in monotremes), a process that produces cone pigments with respective peak sensitivities in the short and middle-to-long wavelengths. With the exception of a number of primate taxa, the modal pattern for mammals is to have two types of cone photopigment, one drawn from each of the gene families. In recent years, it has been discovered that the SWS1 opsin genes of a widely divergent collection of eutherian mammals have accumulated mutational changes that render them nonfunctional. This alteration reduces the retinal complements of these species to a single cone type, thus rendering ordinary color vision impossible. At present, several dozen species from five mammalian orders have been identified as falling into this category, but the total number of mammalian species that have lost short-wavelength cones in this way is certain to be much larger, perhaps reaching as high as 10% of all species. A number of circumstances that might be used to explain this widespread cone loss can be identified. Among these, the single consistent fact is that the species so affected are nocturnal or, if they are not technically nocturnal, they at least feature retinal organizations that are typically associated with that lifestyle. At the same time, however, there are many nocturnal mammals that retain functional short-wavelength cones. Nocturnality thus appears to set the stage for loss of functional SWS1 opsin genes in mammals, but it cannot be the sole circumstance.

The evolution of vertebrate color vision.

Color vision is conventionally defined as the ability of animals to reliably discriminate among objects and lights based solely on differences in their spectral properties. Although the nature of color vision varies widely in different animals, a large majority of all vertebrate species possess some color vision and that fact attests to the adaptive importance this capacity holds as a tool for analyzing the environment. In recent years dramatic advances have been made in our understanding of the nature of vertebrate color vision and of the evolution of the biological mechanisms underlying this capacity. In this chapter I review and comment on these advances.

Characterization of opsin gene alleles affecting color vision in a wild population of titi monkeys (Callicebus brunneus).

The color vision of most platyrrhine primates is determined by alleles at the polymorphic X-linked locus coding for the opsin responsible for the middle- to long-wavelength (M/L) cone photopigment. Females who are heterozygous at the locus have trichromatic vision, whereas homozygous females and all males are dichromatic. This study characterized the opsin alleles in a wild population of the socially monogamous platyrrhine monkey Callicebus brunneus (the brown titi monkey), a primate that an earlier study suggests may possess an unusual number of alleles at this locus and thus may be a subject of special interest in the study of primate color vision. Direct sequencing of regions of the M/L opsin gene using feces-, blood-, and saliva-derived DNA obtained from 14 individuals yielded evidence for the presence of three functionally distinct alleles, corresponding to the most common M/L photopigment variants inferred from a physiological study of cone spectral sensitivity in captive Callicebus.

Cone pigments in a North American marsupial, the opossum (Didelphis virginiana).

Only two of the four cone opsin gene families found in vertebrates are represented in contemporary eutherian and marsupial species. Recent genetic studies of two species of South American marsupial detected the presence of representatives from two of the classes of cone opsin genes and the structures of these genes predicted cone pigments with respective peaks in the ultraviolet and long-wavelength portions of the spectrum. The Virginia opossum (Didelphis virginiana), a profoundly nocturnal animal, is the only marsupial species found in North America. The prospects for cone-based vision in this species were examined through recordings of the electroretinogram (ERG), a commonly examined retinal response to photic stimulation. Recorded under flickering-light conditions that elicit signals from cone photoreceptors, the spectral sensitivity of the opossum eye is well accounted for by contributions from the presence of a single cone pigment having peak absorption at 561-562 nm. A series of additional experiments that employed various chromatic adaptation paradigms were conducted in a search for possible contributions from a second (short-wavelength sensitive) cone pigment. We found no evidence that such a mechanism contributes to the ERG in this marsupial.

The Verriest Lecture 2009: recent progress in understanding mammalian color vision.

There have been significant advances in our understanding of mammalian color vision over the past 15 years. This paper reviews a number of topics that have been central to these recent efforts, including: (1) the extent and nature of ultraviolet vision in mammals, (2) the evolutionary loss of short-wavelength-sensitive cones in some mammals, (3) the possible roles of rod signals in mammalian color vision, (4) the evolution of mammalian color vision, and (5) recent laboratory investigations of animal color vision. Successes in linking opsin genes and photopigments to color vision have been key to the progress made on each of these issues.

Early afferent signaling in the outer plexiform layer regulates development of horizontal cell morphology.

The dendritic patterning of retinal horizontal cells has been shown to be specified by the cone photoreceptor afferents. The present investigation has addressed whether this specification is due to visually dependent synaptic transmission in the outer plexiform layer or to some other early, pre-visual, neural activity. Individually labeled horizontal cells from dark-reared mice, as well as from mice carrying a mutation in the Cacna1f gene, which encodes the pore-forming calcium channel subunit Ca(v)1.4, were assessed for various morphological features. The dark-reared mice showed no alteration in any of these features, despite showing a compromised maximal voltage response in the electroretinograms. The retinas of Cacna1f mutant mice, by contrast, showed conspicuous morphological changes that mimicked the effects observed previously in coneless transgenic mice. These changes were present as early as postnatal day 10, when the shape and density of the cone pedicles appeared normal. Ultrastructurally, however, the pedicles at this early stage, as well as in maturity, lacked synaptic ribbons and the invaginations associated with postsynaptic processes. These results suggest a role for this calcium channel subunit in ribbon assembly in addition to its role in modulating calcium influx and glutamate release. Together, they suggest a complex cascade of interactions between developing cone pedicles and horizontal cell dendrites involving early spontaneous activity, dendritic attraction, ribbon assembly, and pedicle invagination.

Primate color vision: a comparative perspective.

Thirty years ago virtually everything known about primate color vision derived from psychophysical studies of normal and color-defective humans and from physiological investigations of the visual system of the macaque monkey, the most popular of human surrogates for this purpose. The years since have witnessed much progress toward the goal of understanding this remarkable feature of primate vision. Among many advances, investigations focused on naturally occurring variations in color vision in a wide range of nonhuman primate species have proven to be particularly valuable. Results from such studies have been central to our expanding understanding of the interrelationships between opsin genes, cone photopigments, neural organization, and color vision. This work is also yielding valuable insights into the evolution of color vision.

Photopigments and the dimensionality of animal color vision.

Early color-matching studies established that normal human color vision is trichromatic. Subsequent research revealed a causal link between trichromacy and the presence in the retina of three classes of cone photopigments. Over the years, measurements of the photopigment complements of other species have expanded greatly and these are frequently used to predict the dimensionality of an animal's color vision. This review provides an account of how the linkage between the number of active photopigments and the dimensions of human color vision developed, summarizes the various mechanisms that can impact photopigment spectra and number, and provides an across-species survey to examine cases where the photopigment link to the dimensionality of color vision has been claimed. The literature reveals numerous instances where the human model fails to account for the ways in which the visual systems of other animals exploit information obtained from the presence of multiple photopigments in support of their behavior.

Cone-based vision in the aging mouse.

People often experience age-related declines in cone-based visual capacities despite an absence of apparent visual pathology. Although mice are used as models of human visual pathologies associated with aging, little is known about how age impacts vision in animals with disease-free retinas since most studies have heretofore examined relatively young mice. We examined the effects of age on cone-based vision by assessing opsin gene transcription, cone densities, the flicker electroretinogram (ERG), and behavioral increment thresholds in mice. ERG measurements of cone function showed age-related declines in maximum voltage (Vmax), while opsin gene transcription, cone density, and increment thresholds were unchanged even in extremely old mice. The age-related decline in Vmax seen in mice is qualitatively similar to that documented for human subjects. It is notable that Vmax, a commonly used index of ERG activity, does not predict behavioral performance in the mouse.

Cone photoreceptor recovery after experimental detachment and reattachment: an immunocytochemical, morphological, and electrophysiological study.

PURPOSE: To compare the morphologic and functional recovery of the retina after detachment and reattachment in an animal with a cone-dominant retina, the ground squirrel. METHODS: Ground squirrel (Spermophilus beecheyi) retinas were detached for 1 day and reattached for 7, 35, or 96 days (n = 2, each time point). Flicker ERGs were recorded 1 day after the detachment and at various times after reattachment. Contrast-response functions were measured for isochromatic modulation and for selective modulation of short-wavelength-sensitive (S) and middle-wavelength-sensitive (M) cones. At the end of the experiment, retinas were prepared for light microscopy or immunocytochemical staining with antibodies to rod opsin, S and M cone opsins, cytochrome oxidase, synaptophysin, glial fibrillary acidic protein (GFAP), cellular retinaldehyde-binding protein (CRALBP), interphotoreceptor-binding protein (IRBP), and peanut agglutinin lectin (PNA). Photoreceptor density maps were created from wholemount preparations labeled with biotinylated PNA and anti-S cone opsin. Cell counts of photoreceptor nuclei and cone outer segments (OS) were compared with flicker ERG data. Cell death was examined by the TUNEL method. RESULTS: Reattachment stopped photoreceptor cell death and reversed the disruption of interphotoreceptor matrix as well as the redistribution of Müller cell proteins. It also activated some astrocytes based on anti-GFAP staining. S- and M-cone OS showed a gradual recovery in length after reattachment, and this recovery continued to the longest time points examined. ERG contrast gains also recovered after reattachment, but these reached asymptotic levels by approximately a week after reattachment. There were significant correlations between outer nuclear layer (ONL) cell counts and ERG contrast gains. No differences were noted in the indices of recovery of M and S cones. CONCLUSIONS: The ERG can be used to follow specifically the changes in the retina that occur after retinal detachment and reattachment.

Cone pigment variations in four genera of new world monkeys.

Previous research revealed significant individual variations in opsin genes and cone photopigments in several species of platyrrhine (New World) monkeys and showed that these in turn can yield significant variations in color vision. To extend the understanding of the nature of color vision in New World monkeys, electroretinogram flicker photometry was used to obtain spectral sensitivity measurements from representatives of four platyrrhine genera (Cebus, Leontopithecus, Saguinus, Pithecia). Animals from each genus were found to be polymorphic for middle to long-wavelength (M/L) sensitive cones. The presence of a short-wavelength sensitive photopigment was established as well so these animals conform to the earlier pattern in predicting that all male monkeys are dichromats while, depending on their opsin gene array, individual females can be either dichromatic or trichromatic. Across subjects a total of five different M/L cone pigments were inferred with a subset of three of these present in each species.

Influence of cone pigment coexpression on spectral sensitivity and color vision in the mouse.

The mouse retina contains both middle-wavelength-sensitive (M) and ultraviolet-sensitive (UV) photopigments that are coexpressed in cones. To examine some potential visual consequences of cone pigment coexpression, spectral sensitivity functions were measured in mice (Mus musculus) using both the flicker electroretinogram (ERG) and behavioral discrimination tests. Discrimination tests were also employed to search for the presence of color vision in the mouse. Spectral sensitivity functions for the mouse obtained from ERG measurements and from psychophysical tests each reveal contributions from two classes of cone having peak sensitivities (lambda(max)) of approximately 360 and 509-512 nm. The relative contributions of the two pigment types to spectral sensitivity differ significantly in the two types of measurements with a relationship reversed from that often seen in mammals. Mice were capable of discriminating between some pairs of spectral stimuli under test conditions where luminance-related cues were irrelevant. Since mice can make dichromatic color discriminations, their visual systems must be able to exploit differences in the spectral absorption properties among the cones. Complete selective segregation of opsins into individual photoreceptors is apparently not a prerequisite for color vision.

Opsin gene and photopigment polymorphism in a prosimian primate.

A recent genetic investigation found some species of prosimian to have an opsin gene polymorphism [Nature 402 (1999) 36]. In the present study the functional implications of this finding were explored in a correlated investigation of opsin genes and spectral sensitivity measurements of a diurnal prosimian, Coquerel's sifaka (Propithecus verreauxi coquereli). Spectra recorded using electroretinogram (ERG) flicker photometry reveal a cone photopigment polymorphism paralleling an opsin gene polymorphism detected by molecular methods. This species has two middle-to-long-wavelength cone pigments with peak sensitivities of about 545 and 558 nm and a short-wavelength-sensitive cone with a peak at about 430 nm. The distribution of these pigments among animals predicts the presence of both dichromatic and trichromatic forms of color vision.

Photopigments underlying color vision in ringtail lemurs (Lemur catta) and brown lemurs (Eulemur fulvus).

A recent examination of color vision in the ringtail lemur produced evidence that these prosimians could make color discriminations consistent with a diagnosis of trichromatic color vision. However, it was unclear if this behavior reflected the presence of three classes of cone or whether lemurs might be able to utilize signals from rods in conjunction with those from only two classes of cone. To resolve that issue, spectral sensitivity functions were obtained from ringtail lemurs (Lemur catta) and brown lemurs (Eulemur fulvus) using a noninvasive electrophysiological procedure, electroretinographic flicker photometry. Results from experiments involving chromatic adaptation indicate that these lemurs routinely have only a single class of cone photopigment in the middle to long wavelengths (peak sensitivity of about 545 nm); they also have a short-wavelengthsensitive cone pigment with peak of about 437 nm. The earlier behavioral results are suggested to have resulted from the ability of lemurs to jointly utilize signals from rods and cones. The cone pigment complements of these lemurs differ distinctly from those seen among the anthropoids. © 1993 Wiley-Liss, Inc.

Spectral sensitivity and photopigments of a nocturnal prosimian, the bushbaby (Otolemur crassicaudatus).

Earlier studies yielded conflicting conclusions on the types of photoreceptors and photopigments found in the eyes of nocturnal prosimians. In this investigation a noninvasive electrophysiological procedure, electroretinogram flicker photometry, was employed to measure scotopic and photopic spectral sensitivity in the thick-tailed bushbaby (Otolemur crassicaudatus). The scotopic spectral sensitivity function of the bushbaby has a peak of about 507 nm. Under photopic test conditions, spectral sensitivity shifts toward the longer wavelengths. The results from a series of adaptation experiments indicate that the cones of the bushbaby retina contain only a single type of cone photopigment (peak sensitivity at about 545 nm). One implication from this result is that these animals do not have color vision. The photopigment arrangement of the bushbaby is different from that earlier found in diurnal and crepuscular prosimians but is similar to that of the owl monkey, the only nocturnal simian. © 1996 Wiley-Liss, Inc.

Color vision variations in Old and New World primates.

It has long been recognized that there are significant individual variations in color vision among humans. Recently, even more widespread individual variation in color vision has been found to occur in members of several genera of New World monkeys. This article addresses the question of whether a representative genus of Old World monkeys, Macaca, expresses individual variations in color vision. The principal approach was to compare behavioral measurements of increment-threshold spectral sensitivity for large samples of squirrel monkeys (Saimiri sp.) and macaque monkeys (Macaca mulatta, M. fascicularis). We conclude that, if they occur at all, individual variations in color vision among macaque monkeys must be rare.

Spectral sensitivity of vervet monkeys (Cercopithecus aethiops sabaeus) and the issue of catarrhine trichromacy.

Several genera of platyrrhine monkeys show significant polymorphism of color vision. By contrast, catarrhine monkeys have usually been assumed to have uniform trichromatic color vision. However, the evidential basis for this assumption is quite limited. To study this issue further, spectral sensitivity functions were obtained from vervet monkeys (Cercopithecus aethiops sabaeus) using the technique of electroretinographic flicker photometry. Results from a chromatic adaptation experiment indicated that each of the twelve subjects had two classes of cone pigment in the 540/640 nm portion of the spectrum. That result strongly suggests that this species has routine trichromatic color vision. Comparison of the spectral sensitivity functions obtained from vervets and from similarly-tested humans further indicates that the cone complements of the two species are very similar. Results from this investigation add further support to the idea that there are fundamental differences in the genetic mechanisms underlying color vision in platyrrhine and catarrhine monkeys.

Evolution of vertebrate colour vision.

Recent years have witnessed a growing interest in learning how colour vision has evolved. This trend has been fuelled by an enhanced understanding of the nature and extent of colour vision among contemporary species, by a deeper understanding of the paleontological record and by the application of new tools from molecular biology. This review provides an assessment of the progress in understanding the evolution of vertebrate colour vision. In so doing, we offer accounts of the evolution of three classes of mechanism important for colour vision--photopigment opsins, oil droplets and retinal organisation--and then examine details of how colour vision has evolved among mammals and, more specifically, among primates.

The discovery of spectral opponency in visual systems and its impact on understanding the neurobiology of color vision.

The two principal theories of color vision that emerged in the nineteenth century offered alternative ideas about the nature of the biological mechanisms that underlie the percepts of color. One, the Young-Helmholtz theory, proposed that the visual system contained three component mechanisms whose individual activations were linked to the perception of three principal hues; the other, the Hering theory, assumed there were three underlying mechanisms, each comprising a linked opponency that supported contrasting and mutually exclusive color percepts. These competing conceptions remained effectively untested until the middle of the twentieth century when single-unit electrophysiology emerged as a tool allowing a direct examination of links between spectral stimulation of the eye and responses of individual cells in visual systems. This approach revealed that the visual systems of animals known to have color vision contain cells that respond in a spectrally-opponent manner, firing to some wavelengths of stimulation and inhibiting to others. The discovery of spectral opponency, and the research it stimulated, changed irrevocably our understanding of the biology of color vision.