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Journal ArticleDOI

Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments

TL;DR: Good quantitative agreement was found when the microspectrophoto-metrically measured absorbance spectra were used to predict the behavioural sensitivity of individual animals to long wavelengths and suggests that the behavioural variation arises from variation in the retinal photopigments.
Abstract: The squirrel monkey (Saimiri sciureus) exhibits a polymorphism of colour vision: some animals are dichromatic, some trichromatic, and within each of these classes there are subtypes that resemble the protan and deutan variants of human colour vision. For each of ten individual monkeys we have obtained (i) behavioural measurements of colour vision and (ii) microspectrophotometric measurements of retinal photopigments. The behavioural tests, carried out in Santa Barbara, included wavelength discrimination, Rayleigh matches, and increment sensitivity at 540 and 640 nm. The microspectrophotometric measurements were made in London, using samples of fresh retinal tissue and a modified Liebman microspectrophotometer: the absorbance spectra for single retinal cells were obtained by passing a monochromatic measuring beam through the outer segments of individual rods and cones. The two types of data, behavioural and microspectrophotometric, were obtained independently and were handed to a third party before being interchanged between experimenters. From all ten animals, a rod pigment was recorded with $\lambda \_{\max}$ (wavelength of peak absorbance) close to 500 nm. In several animals, receptors were found that contained a short-wave pigment (mean $\lambda \_{\max}$ = 433.5 nm): these violet-sensitive receptors were rare, as in man and other primate species. In the middle- to long-wave part of the spectrum, there appear to be at least three possible Saimiri photopigments (with $\lambda \_{\max}$ values at about 537, 550 and 565 nm) and individual animals draw either one or two pigments from this set, giving dichromatic or trichromatic colour vision. Thus, those animals that behaviourally resembled human protanopes exhibited only one pigment in the red--green range, with $\lambda \_{\max}$ = 537 nm; other behaviourally dichromatic animals had single pigments lying at longer wavelengths and these were the animals that behaviourally had higher sensitivity to long wavelengths. Four of the monkeys were behaviourally judged to be trichromatic. None of the latter animals exhibited the two widely separated pigments (close to 535 and 567 nm) that are found in the middle- and long-wave cones of macaque monkeys. But the spread of $\lambda \_{\max}$ values for individual cones was greater in the trichromatic squirrel monkeys than in the dichromats; than in the case of three, behaviourally deuteranomalous, trichromats there was clear evidence that the distribution of $\lambda \_{\max}$ values was bimodal, suggesting photopigments at approximately 552 and 565 nm. The fourth, behaviourally protanomalous, trichromat exhibited a spread of individual $\lambda _{\max}$ values that ranged between 530 and 550 nm. Good quantitative agreement was found when the microspectrophotometrically measured absorbance spectra were used to predict the behavioural sensitivity of individual animals to long wavelengths. The concordance of the two sets of measurements places beyond question the existence of a polymorphism of colour vision in Saimiri sciureus and suggests that the behavioural variation arises from variation in the retinal photopigments. Heterozygous advantage may explain the polymorphism.
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Journal ArticleDOI
TL;DR: This review has evaluated the proposition that relatively few mammalian species have a capacity for colour vision in mammals in the light of recent research on colour vision and its mechanisms in mammals and concluded that the baseline mammalian colour vision is argued to be dichromacy.
Abstract: 1. An oft-cited view, derived principally from the writings of Gordon L. Walls, is that relatively few mammalian species have a capacity for colour vision. This review has evaluated that proposition in the light of recent research on colour vision and its mechanisms in mammals. 2. To yield colour vision a retina must contain two or more spectrally discrete types of photopigment. While this is a necessary condition, it is not a sufficient one. This means, in particular, that inferences about the presence of colour vision drawn from studies of photopigments, the precursors of photopigments, or from nervous system signals must be accepted with due caution. 3. Conjoint signals from rods and cones may be exploited by mammalian nervous systems to yield behavioural discriminations consistent with the formal definition of colour vision. Many mammalian retinas are relatively cone-poor, and thus there are abundant opportunities for such rod/cone interactions. Several instances were cited in which animals having (apparently) only one type of cone photopigment succeed at colour discriminations using such a mechanism. it is suggested that the exploitation of such a mechanism may not be uncommon among mammals. 4. Based on ideas drawn from natural history, Walls (1942) proposed that the receptors and photopigments necessary to support colour vision were lost during the nocturnal phase of mammalian history and then re-acquired during the subsequent mammalian radiations. Contemporary examination of photopigment genes along with the utilization of better techniques for identifying rods and cones suggest a different view, that the earliest mammals had retinas containing some cones and two types of cone photopigment. Thus the baseline mammalian colour vision is argued to be dichromacy. 5. A consideration of the broad range of mammalian niches and activity cycles suggests that many mammals are active during photic periods that would make a colour vision capacity potentially useful. 6. A systematic survey was presented that summarized the evidence for colour vision in mammals. Indications of the presence and nature of colour vision were drawn both from direct studies of colour vision and from studies of those retinal mechanisms that are most closely associated with the possession of colour vision. Information about colour vision can be adduced for species drawn from nine mammalian orders.(ABSTRACT TRUNCATED AT 400 WORDS)

682 citations

Journal ArticleDOI
TL;DR: It is argued that the colour vision of man and of the Old World monkeys depends on two subsystems that remain parallel and independent at early stages of the visual pathway, and that the New World monkeys have taken a different route to trichromacy.
Abstract: The disabilities experienced by colour-blind people show us the biological advantages of colour vision in detecting targets, in segregating the visual field and in identifying particular objects or states. Human dichromats have especial difficulty in detecting coloured fruit against dappled foliage that varies randomly in luminosity; it is suggested that yellow and orange tropical fruits have co-evolved with the trichromatic colour vision of Old World monkeys. It is argued that the colour vision of man and of the Old World monkeys depends on two subsystems that remain parallel and independent at early stages of the visual pathway. The primordial subsystem, which is shared with most mammals, depends on a comparison of the rates of quantum catch in the short- and middle-wave cones; this system exists almost exclusively for colour vision, although the chromatic signals carry with them a local sign that allows them to sustain several of the functions of spatiochromatic vision. The second subsystem arose from the phylogenetically recent duplication of a gene on the X-chromosome, and depends on a comparison of the rates of quantum catch in the long- and middle-wave receptors. At the early stages of the visual pathway, this chromatic information is carried by a channel that is also sensitive to spatial contrast. The New World monkeys have taken a different route to trichromacy: in species that are basically dichromatic, heterozygous females gain trichromacy as a result of X-chromosome inactivation, which ensures that different photopigments are expressed in two subsets of retinal photoreceptor.

559 citations


Cites background from "Variations of colour vision in a Ne..."

  • ...…therefore added sparingly to the retinal matrix, and they remain rare: they constitute only a few per cent of all cones in every primate species where cones have been identified directly by microspectrophotometry (e.g. Bowmaker et al. 1987; Harosi, 1982; Dartnall et al. 1983; Mollon et al. 1984)....

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  • ...These findings have been explained by a genetic model (Mollon etal....

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  • ...In a double-blind study that combined behavioural testing and microspectrophotometry (Mollon et al. 1984; Bowmaker et al. 1987), six phenotypes were identified in the squirrel monkey (Saimiri sciureus): all males and some females were dichromats, combining a short-wave pigment with one of three…...

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Journal ArticleDOI
TL;DR: Both molecular evolutionary analyses of visual pigments and vision science have an important common goal to understand the molecular mechanisms involved in functional adaptations of organisms to different environments, including the mechanisms of the regulation of the spectral absorption.

535 citations

Journal ArticleDOI
TL;DR: It is reported that particular trichromatic platyrrhine phenotypes may be better suited than others to foraging for particular fruits under particular conditions of illumination, and possible explanations for the maintenance of polymorphic colour vision amongst the platyr rhines are discussed.
Abstract: Primates are apparently unique amongst the mammals in possessing trichromatic colour vision. However, not all primates are trichromatic. Amongst the haplorhine (higher) primates, the catarrhines possess uniformly trichromatic colour vision, whereas most of the platyrrhine species exhibit polymorphic colour vision, with a variety of dichromatic and trichromatic phenotypes within the population. It has been suggested that trichromacy in primates and the reflectance functions of certain tropical fruits are aspects of a coevolved seed-dispersal system: primate colour vision has been shaped by the need to find coloured fruits amongst foliage, and the fruits themselves have evolved to be salient to primates and so secure dissemination of their seeds. We review the evidence for and against this hypothesis and we report an empirical test: we show that the spectral positioning of the cone pigments found in trichromatic South American primates is well matched to the task of detecting fruits against a background of leaves. We further report that particular trichromatic platyrrhine phenotypes may be better suited than others to foraging for particular fruits under particular conditions of illumination; and we discuss possible explanations for the maintenance of polymorphic colour vision amongst the platyrrhines.

515 citations


Cites background from "Variations of colour vision in a Ne..."

  • ...These studies ( Jacobs et al. 1981; Mollon et al. 1984; Bowmaker et al. 1987) found an S cone pigment in the population with a peak sensitivity at around 433 nm, and three di¡erent M or L cone pigments with peak sensitivities at 536, 550 and 564 nm. Monkeys diagnosed behaviourally as dichromats…...

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  • ...An explanation for the polymorphic colour vision of the squirrel monkey was given by Mollon et al. (1984), who suggested that there is a single X-chromosome locus for an M or L cone pigment Phil....

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  • ...The polymorphism of platyrrhine monkeys might then be maintained by frequency-dependent advantage (Clarke 1979; Mollon et al. 1984): the advantage of the individual dichromat in certain foraging tasks over trichromatic conspeci¢cs....

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  • ...It is therefore possible that the most successful groups contain a variety of di¡erent dichromatic and trichromatic individuals, each with advantages and disadvantages at particular foraging tasks, and that the maintenance of polymorphic colour vision in platyrrhine monkeys is by kin selection, giving a net group bene¢t for the detection of resources (Mollon et al. 1984)....

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  • ...In platyrrhine species with polymorphic colour vision, the variation among dichromatic males may simply be maintained by heterozygous advantage (Mollon et al. 1984): the advantage of trichromatic females at detecting fruits and conspeci¢cs against a background of foliage....

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Journal ArticleDOI
TL;DR: Microspectrophotometric examination of the retinal photoreceptors of the budgerigar, Melopsittacus undulatus (Psittaciformes) and the zebra finch and the Taeniopygia guttata (Passeriformes), demonstrate the presence of four, spectrally distinct classes of single cone that contain visual pigments absorbing maximally at about 565, 507, 430-445 and 360-380 nm.

484 citations


Cites methods from "Variations of colour vision in a Ne..."

  • ...The absorbance spectra of individual photoreceptors were measured with a modified dual-beam Liebman microspectrophotometer under computer control (Liebman & Entine, 1964; Knowles & Dartnall, 1977; Mollon et al., 1984; Bowmaker et al., 1991a)....

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