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.

X-linked photopigment polymorphism produces six different color vision phenotypes in most species of New World monkey. In the subfamily Callitrichinae, the three M/L alleles underlying these different phenotypes are present at unequal frequencies suggesting that selective pressures other than heterozygous-advantage operate on these alleles. Earlier we investigated this hypothesis with functional substitution, a technique using a computer monitor to simulate colors as they would appear to humans with monkey visual pigments (Visual Neuroscience21:217–222, 2004). The stimuli were derived from measurements of ecologically relevant fruit and foliage. We found that discrimination performance depended on the relative spectral positioning of the substituted M and L pigment pair. Here we have undertaken a systematic examination of two simulation parameters—test field luminance and stimulus duration. Discriminability of the fruit colors depended on which phenotype was simulated but only at short stimulus durations and/or low luminances. Under such conditions, phenotypes with the larger pigment peak separations performed better. At longer durations and higher luminances, differences in performance across different substitutions tended to disappear. The stimuli used in this experiment were analyzed with several color discrimination models. There was limited agreement among the predictions made by these models regarding the capabilities of animals with different pigment pairs and none predicted the dependence of discrimination on changes in luminance and stimulus duration.

Most platyrrhine monkeys have a triallelic M/L opsin gene polymorphism that underlies significant individual variations in color vision. A survey of the frequencies of these polymorphic genes suggests that the three alleles occur with equal frequency among squirrel monkeys (subfamily Cebinae), but are not equally frequent in a number of species from the subfamily Callitrichinae. This departure from equal frequency in the Callitrichids should slightly increase the ratio of dichromats to trichromats in the population and significantly alter the relative representation of the three possible dichromatic and trichromatic phenotypes. A particular feature of the inequality is that it leads to a relative increase in the number of trichromats whose M/L pigments have the largest possible spectral separation. To assess whether these trichromatic phenotypes are equally well equipped to make relevant visual discriminations, psychophysical experiments were run on human observers. A technique involving the functional substitution of photopigments was used to simulate the discrimination between fruits among a background of leaves. The goal of the simulation was to reproduce in the cones of human observers excitations equivalent to those produced in monkey cones as the animals view fruit. Three different viewing conditions were examined involving variations in the relative luminances of fruit and leaves and the spectrum of the illuminant. In all cases, performance was best for simulated trichromacies including M/L pigments with the largest spectral separation. Thus, the inequality of opsin gene frequency in Callitrichid monkeys may reflect adaptive pressures.

Much has been learned from studies of Limulus photoreceptors about the role of the circadian clock and light in the removal of photosensitive membrane. However, little is known in this animal about mechanisms regulating photosensitive membrane renewal, including the synthesis of proteins in, and associated with, the photosensitive membrane. To begin to understand renewal, this study examines diurnal changes in the levels of mRNAs encoding opsin, the integral membrane protein component of visual pigment, and the relative roles of light and the circadian clock in producing these changes. We show that at least two distinct opsin genes encoding very similar proteins are expressed in both the lateral and ventral eyes, and that during the day and night in the lateral eye, the average level of mRNA encoding opsin1 is consistently higher than that encoding opsin2. Northern blot assays showed further that total opsin mRNA in the lateral eyes of animals maintained under natural illumination increases during the afternoon (9 & 12 h after sunrise) in the light and falls at night in the dark. This diurnal change occurs whether or not the eyes receive input from the circadian clock, but it is eliminated in eyes maintained in the dark. Thus, it is regulated by light and darkness, not by the circadian clock, with light stimulating an increase in opsin mRNA levels. The rise in opsin mRNA levels observed under natural illumination was seasonal; it occurred during the summer but not the spring and fall. However, a significant increase in opsin mRNA levels could be achieved in the fall by exposing lateral eyes to 3 h of natural illumination followed by 9 h of artificial light. The diurnal regulation of opsin mRNA levels contrasts sharply with the circadian regulation of visual arrestin mRNA levels (Battelle et al., 2000). Thus, in Limulus, distinctly different mechanisms regulate the levels of mRNA encoding two proteins critical for the photoresponse.