Trichromatic Females Research Articles

Analysis of the lateral geniculate nucleus in dichromatic and trichromatic marmosets.

Marmosets are diurnal New World monkeys that show sex-linked cone photopigment polymorphism, whereby all males and some females are dichromats ("red-green colorblind"), but most females show trichromatic color vision. Here we asked whether trichromats express chromatic-specific circuitry in the lateral geniculate nucleus (LGN). The volume of parvocellular (P), magnocellular (M), and koniocellular (K) layers was calculated in Nissl-stained sections from the LGN of adult marmosets (Callithrix jacchus; 10 trichromatic females; 2 dichromatic females; and 13 dichromatic males). Retinal ganglion cell axon terminals within the P and K layers were reconstructed and measured following anterograde tracer (dextran) injections. We show that there is little difference in LGN layer volume with respect to age, weight, or sex of the animals, or between dichromatic and trichromatic phenotypes. The morphology of retinal ganglion cell terminals was largely indistinguishable on comparing dichromats and trichromats, and likewise on comparing terminals representing peripheral or foveal retina. We conclude that the LGN circuits we studied are largely independent of red-green color vision phenotype and visual field location.

Incorporating ecology and social system into formal hypotheses to guide field studies of color vision in primates

The X-linked gene polymorphism responsible for the variable color vision of most Neotropical monkeys and some lemurs is thought to be maintained by balancing selection, such that trichromats have an advantage over dichromats for some ecologically important task(s). However, evidence for such an advantage in wild primate populations is equivocal. The purpose of this study is to refine a hypothesis for a trichromat advantage by tailoring it to the ecology of territorial primates with female natal dispersal, such that dispersing trichromatic females have a foraging and, by extension, survival advantage over dichromats. I then examine the most practical way to test this hypothesis using field data. Indirect evidence in support of the hypothesis may take the form of differences in genotype frequencies among life stages and differences in disperser food item encounter rates. A deterministic evolutionary matrix population model and a stochastic model of food patch encounter rates are constructed to investigate the magnitude of such differences and the likelihood of statistical detection using field data. Results suggest that, although the sampling effort required to detect the hypothesized genotype frequency differences is impractical, a field study of reasonable scope may be able to detect differences in disperser foraging rates. This study demonstrates the utility of incorporating socioecological details into formal hypotheses during the planning stages of field studies of primate color vision.

Color Vision Variation and Foraging Behavior in Wild Neotropical Titi Monkeys (Callicebus brunneus): Possible Mediating Roles for Spatial Memory and Reproductive Status

The selective advantages to primates of trichromatic color vision, allowing discrimination among the colors green, yellow, orange, and red, remain poorly understood. We test the hypothesis that, for primates, an advantage of trichromacy over dichromacy, in which such colors are apt to be confused, lies in the detection of yellow, orange, or red (YOR) food patches at a distance, while controlling for the potentially confounding influences of reproductive status and memory of food patch locations. We employ socially monogamous titi monkeys (Callicebus brunneus) which, like most platyrrhine primates, have polymorphic color vision resulting in populations containing both dichromatic and trichromatic individuals. Wild Callicebus brunneus spent most foraging time in YOR food patches, the locations of most of which were likely to have been memorable for the subjects. Overall, both dichromatic and trichromatic females had significantly higher encounter rates than their dichromatic male pair mates for low-yield ephemeral YOR food patches whose locations were less likely to have been remembered. We detected no difference in the encounter rates of dichromatic and trichromatic females for such patches. However, the data suggest that such a difference may be detectable with a larger sample of groups of Callicebus brunneus, a larger sample of foraging observations per group, or both. We propose that a trichromatic advantage for foraging primates may be realized only when individuals’ energy requirements warrant searching for nonmemorable YOR food patches, a context for selection considerably more limited than is often assumed in explanations of the evolution of primate color vision.

Poorer color discrimination by females when tested with pseudoisochromatic plates containing vanishing designs on neutral backgrounds

It might be expected that normal trichromatic females would perform as well as normal trichromatic males of the same age when tested with standard clinical color-vision tests that use pseudoisochromatic vanishing designs on neutral gray backgrounds such as the Hardy-Rand-Rittler (HRR) pseudoisochromatic plates and the Neitz Test of Color Vision (NTCV). Here 2966 children aged 6-13 years from four municipalities in Norway were tested in their school classrooms with the NTCV. Children who made errors on the test were retested. 187 males and 152 females made one or more errors on retest, and each was tested individually on the Richmond HRR Fourth Edition. 8% of the males were defined as color deficient when a double criterion for failing was applied, that is, one or more errors on the NTCV and two or more errors on the HRR. The calculated frequency of color-deficient females (homozygotes) for the same criterion is 0.42%. By contrast, 3% of females failed the criterion that gave a stable population of color-deficient males. This result is considered in relation to reports of female carriers of color-vision deficiency having problems with the Ishihara test and of females having poorer color discrimination than males.

Effect of color vision phenotype on the foraging of wild white-faced capuchins, Cebus capucinus

New World monkeys exhibit a color vision polymorphism. It results from allelic variation of the single-locus middle-to-long wavelength opsin gene on the X chromosome. Females that are heterozygous for the gene possess trichromatic vision. All other individuals possess dichromatic vision. The prevailing hypothesis for the maintenance of the color vision polymorphism is through a consistent fitness advantage to heterozygous trichromatic females. Such females are predicted to be more efficient than dichromats when detecting and selecting fruit. Recent experiments with captive callitrichid primates provided support for this hypothesis by demonstrating that color vision phenotype affects behavioral responses to contrived food targets. Yet, the assumptions that trichromatic females acquire more calories from fruit, or that number of offspring is linked to caloric intake, remain untested. Here, we assess if, in the wild, heterozygous trichromatic individuals in a group of white-faced capuchins (Cebus capucinus) enjoy an energetic advantage over dichromats when foraging on fruit. Contrary to the assumptions of previous theoretical and experimental studies, our analysis of C. capucinus foraging behavior shows that trichromats do not differ from dichromats in their fruit or energy acquisition rates. For white-faced capuchins, the advantage of trichromatic vision may be related to the detection of predators, animal prey, or fruit under mesopic conditions. This result demonstrates the importance of using a fitness currency that is relevant to individual animals to test evolutionary hypotheses.

Color vision pigment frequencies in wild tamarins (Saguinusspp.)

The adaptive importance of polymorphic color vision found in many New World and some prosimian primates has been discussed for many years. Polymorphism is probably maintained in part through a heterozygote advantage for trichromatic females, as such individuals are observed to have greater foraging success when selecting ripe fruits against a background of forest leaves. However, recent work also suggests there are some situations in which dichromatic individuals may have an advantage, and that variation in color vision among individuals possessing different alleles may also be significant. Alleles that confer a selective advantage to individuals are expected to occur at a higher frequency in populations than those that do not. Therefore, analyzing the frequencies of color vision alleles in wild populations can add to our understanding of the selective advantages of some color vision phenotypes over others. With this aim, we used molecular techniques to determine the frequencies of color vision alleles in 12 wild tamarin groups representing three species of the genus Saguinus. Our results show that allele frequencies are not equal, possibly reflecting different selective regimes operating on different color vision phenotypes.

Non-random association of opsin alleles in wild groups of red-bellied tamarins (Saguinus labiatus) and maintenance of the colour vision polymorphism.

The remarkable X-linked colour vision polymorphism observed in many New World primates is thought to be maintained by balancing selection. Behavioural tests support a hypothesis of heterozygote advantage, as heterozygous females (with trichromatic vision) exhibit foraging benefits over homozygous females and males (with dichromatic vision) when detecting ripe fruit on a background of leaves. Whilst most studies to date have examined the functional relevance of polymorphic colour vision in the context of foraging behaviour, alternative hypotheses proposed to explain the polymorphism have remained unexplored. In this study we examine colour vision polymorphism, social group composition and breeding success in wild red-bellied tamarins Saguinus labiatus. We find that the association of males and females within tamarin social groups is non-random with respect to colour vision genotype, with identified mating partners having the greatest allelic diversity. The observed distribution of alleles may be driven by inbreeding avoidance and implies an important new mechanism for maintaining colour vision polymorphism. This study also provides the first preliminary evidence that wild trichromatic females may have increased fitness compared with dichromatic counterparts, as measured by breeding success and longevity.

Colour Discrimination in the Black-Tufted-Ear Marmoset (Callithrix penicillata): Ecological Implications

The dietary diversity of marmosets is substantial, which may reflect differences in their colour vision. This study examined the colour discrimination ability of a gummivore/insectivore callitrichid, Callithrix penicillata, which inhabits the Brazilian cerrado (bush savanna). A series of ecologically relevant tasks, involving a behavioural paradigm of discrimination learning in semi-natural conditions and the usage of ecologically relevant stimuli, was executed. Three marmosets, 2 males and a female, behaved like human dichromats, showing an impaired performance when orange and green stimuli had to be discriminated. In contrast, 2 females resembled human trichromats, discriminating those kinds of pairs. Our data suggest that Callithrix penicillata presents a polymorphic trichromacy, with dichromatic males and dichromatic or trichromatic females.

Color Vision in Leontopithecus chrysomelas: A Behavioral Study

We assessed the color discriminations by golden-headed lion tamarins (Leontopithecus chrysomelas) via a series of tasks involving a behavioral paradigm that maximizes the naturalness of the stimuli. The stimuli were pairs of Munsell color chips used in earlier experiments with human dichromats. We tested 3 male and 3 female monkeys with stimuli of random brightness values in order to assure that discriminations were based on color rather than brightness cues. Results indicate that each male and one female presented random performances for stimuli resembling hue conditions under which tamarins forage: oranges vs. greens. Two females exhibited discriminations consistent with allelic trichromacy. Findings indicate the presence of an M/L cone opsin polymorphism, a condition of most platyrrhines that is characterized by dichromatic and/or trichromatic females and dichromatic males. Interspecific differences in allelic frequency among lion tamarins raises the possibility that habitat fragmentation is affecting heterozygous frequencies, a trend that could impact tamarin foraging efficiency.

Visual responses in the lateral geniculate nucleus of dichromatic and trichromatic marmosets (Callithrix jacchus)

New-world primates such as the marmoset (Callithrix jacchus) show polymorphism for the middle- to long-wavelength sensitive cone pigments. Each X-chromosome carries a gene for only one of three possible pigments. All males are thus dichromats, but some females will be trichromats. We have investigated the responses of cells of the parvocellular (PC) and magnocellular (MC) systems within animals from a single marmoset family. The middle- to long-wavelength pigment of dichromats was identified physiologically. Trichromats could readily be distinguished from dichromats by the presence of a high proportion of red-green opponent PC-cells. The physiological classification of phenotypes was confirmed with genetic analysis. The pattern of inheritance was consistent with current genetic models. In trichromatic females, the properties of cells resembled in detail those of cells from the PC- and MC-pathways of the macaque. In dichromats, cell responses resembled those of trichromats (except for the lack of opponency in PC-cells); PC-cells showed sustained and MC-cells transient responses, with a lower contrast gain for the former type. One difference was that a proportion of PC-cells in dichromats showed strong rod input even at high levels of retinal illuminance. Thus, in trichromatic marmosets the presence of two middle- to long-wave pigments appears to permit the elaboration of all the physiological properties associated with trichromacy.

Polymorphism of photopigments in the squirrel monkey: a sixth phenotype.

We describe here a trichromatic type of squirrel monkey that resembles Old World monkeys in having two well-separated photopigments in the red-green part of the spectrum; the cones of this phenotype have peak sensitivities close to 430, 536 and 564 nm. The existence of such animals is predicted by a genetic model that postulates three alleles for a single locus on the X-chromosome of the squirrel monkey. The three alleles correspond to three different photopigments in the red-green spectral range. A male monkey, or a homozygous female, will be dichromatic, combining short-wave cones with just one of the cone types in the red-green range. But a female monkey, if heterozygous at the locus, draws any two of the three alleles from the set. X-chromosome inactivation ensures that the two alleles are expressed in different subpopulations of retinal cone, giving the monkey the basis for trichromatic colour vision. This model requires three trichromatic types of female squirrel monkey. The photopigment complements of two types have previously been reported and microspectrophotometric data are now given for the third type. Behaviourally, this third type of trichromat gives precise Rayleigh matches that are intermediate between those of the other two types of trichromat. The polymorphism of photopigments in the squirrel monkey may be maintained by the heterozygous advantage enjoyed by the trichromatic females. This would be an instructive instance of heterozygous advantage because it is a case where X-chromosome inactivation plays a crucial role in segregating the two different gene-products into different cells.