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Vertebrate color vision is an ideal system for studying the gains and losses of genetic variation across lineages and impacts on behavior. Among placental mammals, trichromatic vision is unique to primates and is argued to be adaptive for foraging on reddish food. However, trichromacy is variably present in lemurs, including species within the cathemeral genus Eulemur, due to inter- and intra-specific variation in X-linked opsin genes. Although this variation could result from genetic drift, it could also reflect ecological adaptation. To understand ecological contributions to color vision variation, we examined cone opsin genes of 11 Eulemur species. We found that only E. flavifrons and E. macaco have polymorphic trichromacy. Most dichromatic species have an “M” (green-shifted) opsin; uniquely, one species (E. rubriventer) has dichromacy based on an “L” (red-shifted) opsin. This latter result appears to represent loss of polymorphic trichromacy from a dichromatic (M opsin) or polymorphic Eulemur ancestor. To address potential ecological explanations for opsin variation, we studied the dietary behavior of wild E. rubriventer and collected reflectance spectra from plant species consumed. Visual models suggest that trichromacy should provide an advantage for detecting reddish foods; however, luminance contrasts were greatest for dichromats with the L opsin. As E. rubriventer are often active in low-light rainforest conditions, luminance cues may be relatively important, which could favor the L opsin, while also leading to relaxed selection on, or selection against, trichromacy. The presence of different opsin alleles across Eulemur species could represent adaptations related to diet, activity pattern, or habitat. Loss of genetic variation, often thought to be maladaptive, can occur through natural selection. Among primates, some species have trichromatic color vision, the ability to distinguish reddish and greenish hues; others are red-green colorblind (dichromatic). We examined adaptive explanations for color vision differences by studying cone opsin genes and behavior in wild lemurs (Eulemur)—a genus that is active both day and night. We found that color vision is variable in Eulemur species, and full trichromatic vision was likely lost in at least one lineage. Foraging ecology of dichromatic Eulemur rubriventer indicates that trichromatic vision should be advantageous for foraging on reddish foods, but brightness cues are more salient to this species’ vision. We suggest brightness may be more important than color to this species, particularly at night, and loss of trichromacy could be adaptive in some lemurs.

Many plants use colour to attract pollinators, which often possess colour vision systems well-suited for detecting flowers. Yet, to isolate the role of colour is difficult, as flowers also produce other cues. The study of florivory by Neotropical primates possessing polymorphic colour vision provides an opportunity to investigate the importance of colour directly. Here we determine whether differences in colour vision within a mixed population of wild dichromatic and trichromatic white-faced capuchins (Cebus capucinus imitator) affect flower foraging behaviours. We collected reflectance data for flower foods and modelled their chromatic properties to capuchin colour vision phenotypes. We collected behavioural data over 22 months spanning four years, determined the colour vision phenotype of each monkey based on amino acid variation of the L/M opsin gene from fecal DNA, and compared foraging behaviours of dichromats and trichromats. Most flowers were more conspicuous to trichromats, and trichromats foraged in small flower patches significantly more often. These data demonstrate a difference in wild primate foraging patterns based on colour vision differences, supporting the hypothesis that trichromacy enhances detection of small, ephemeral resources. This advantage, which may also extend to other foods, likely contributes to the maintenance of colour vision polymorphism in Neotropical monkeys.

The century-old idea that stripes make zebras cryptic to large carnivores has never been examined systematically. We evaluated this hypothesis by passing digital images of zebras through species-specific spatial and colour filters to simulate their appearance for the visual systems of zebras’ primary predators and zebras themselves. We also measured stripe widths and luminance contrast to estimate the maximum distances from which lions, spotted hyaenas, and zebras can resolve stripes. We found that beyond ca. 50 m (daylight) and 30 m (twilight) zebra stripes are difficult for the estimated visual systems of large carnivores to resolve, but not humans. On moonless nights, stripes are difficult for all species to resolve beyond ca. 9 m. In open treeless habitats where zebras spend most time, zebras are as clearly identified by the lion visual system as are similar-sized ungulates, suggesting that stripes cannot confer crypsis by disrupting the zebra’s outline. Stripes confer a minor advantage over solid pelage in masking body shape in woodlands, but the effect is stronger for humans than for predators. Zebras appear to be less able than humans to resolve stripes although they are better than their chief predators. In conclusion, compared to the uniform pelage of other sympatric herbivores it appears highly unlikely that stripes are a form of anti-predator camouflage.

Figs are important resources for frugivores, and Ficus is an ideal taxon for evaluating patterns of primate foraging related to food color. Ficus spp. can be classified as conspicuous (color change from greenish to reddish during ripening) or cryptic (green throughout ripening). To investigate the effect on foraging of color vision phenotype variation for these 2 types of figs, we conducted a 20-mo study on 4 groups of white-faced capuchins (Cebus capucinus) in the Santa Rosa Sector of the ACG, Costa Rica between May 2004 and September 2008. We genotyped all individuals and collected behavioral data on feeding rates, acceptance indices, and foraging sequences. We found a significant effect of fig type; feeding rates and acceptance indices were higher for conspicuous figs than for cryptic figs, and subjects sniffed cryptic figs more often than conspicuous figs. We also found that dichromats sniffed more figs and had longer foraging sequences than trichromats, especially for cryptic figs. Among 6 subtypes of dichromats and trichromats, monkeys possessing the trichromat phenotype with the most spectrally separated L-M opsin alleles showed the highest acceptance index for conspicuous figs, though there were no differences in feeding rates among phenotypes. We conclude: 1) conspicuous figs are visually salient not only for trichromats but also for dichromats, 2) olfaction is important for evaluating edibility of cryptic figs, and 3) the reliance on olfaction for selecting fruit is greater in dichromats. These results indicate divergent foraging strategies among color vision phenotypes for assessing food items.

It is not well understood how primates combine olfactory and visual cues in their natural behaviour, especially during feeding. In this study we conducted field observations of a group of wild, frugivorous black-handed spider monkeys, Ateles geoffroyi (Platyrrhini), consisting of both dichromats (N = 11) and trichromats (N = 9) in Santa Rosa National Park, Costa Rica. We focused on the fruit foraging behaviour, for which involvement of vision has been well studied. We examined how often the monkeys inspected fruits by sniffing them during their fruit feeding attempts (i.e. sniffing index). We found that both dichromats and trichromats sniffed the visually cryptic fruit species more often than the conspicuous species, with the sniffing index being negatively correlated with the luminance and blue–yellow contrasts of fruits to background leaves. Furthermore, the sniffing index was negatively correlated with the proportion of fruits eaten (versus rejected) following a foraging attempt in both dichromats and trichromats. These results suggest that monkeys use olfaction for discrimination between edible and inedible fruits when vision alone is insufficient to evaluate the quality of fruits, showing the first documentation of interplay between vision and olfaction in primate feeding behaviour under natural conditions.

Many species of platyrrhine primates are characterised by sex-linked color vision polymorphism. This presents an opportunity to study the biology and ecology of individuals with different phenotypes living in the same group. Several evolutionary processes could maintain polymorphic genes in populations. In this study, we evaluate the hypothesis that foraging niche divergence among monkeys explains the presence of multiple color vision phenotypes. Specifically, we test whether dichromats and trichromats differ in foraging time devoted to cryptic vs brightly colored resources. We did not find any differences in foraging time spent on different food types by dichromatic and trichromatic monkeys in two groups of white-faced capuchins (Cebus capucinus) living in a tropical dry forest. We conclude that in so far as these variables are concerned, niche divergence does not likely explain color vision polymorphism in our study population.

Unlike most eutherian mammals, which have dichromatic (two-colour) vision, most platyrrhine primate species have polymorphic colour vision. This unique characteristic is enabled via multiple alleles for a midto long-wavelength-sensitive (M/LWS), single-locus opsin gene on the X chromosome. In combination with the autosomal opsin common to most vertebrates, this arrangement provides heterozygous females with trichromatic (three-colour) vision, whereas homozygous females and males are dichromats. Trichromatic vision enables visual differentiation among longer-wavelength colours, such as red, orange, yellow and green. Currently, many researchers attribute the evolution and maintenance of polymorphic colour vision to trichromat (¼ heterozygote) advantage. However, dichromacy may be more suited for achromatic tasks, such as penetrating colour camouflage, especially under low-light conditions. We evaluated whether dichromatic capuchin monkeys (Cebus capucinus) were more efficient than trichromatic monkeys at capturing camouflaged and noncamouflaged insects. Through faecal DNA analysis, we determined the genotypes of the M/LWS opsins for 34 capuchins in two groups inhabiting Santa Rosa National Park, Costa Rica. Dichromatic monkeys were more efficient at detecting camouflaged, surface-dwelling insects, especially under conditions of low ambient light. However, unexpectedly, trichromats were more efficient in extracting embedded, noncamouflaged insects from substrates. To our knowledge, this is the first study to document a foraging advantage to dichromatic monkeys in the wild. Our findings show that there is a lack of heterozygote advantage in foraging for surface-dwelling insects and therefore indicate that this mechanism may not be the sole driving force maintaining polymorphic colour vision in this population.

Due to a middle- to long-wavelength-sensitive (M/LWS) cone opsin polymorphism, there is considerable phenotypic variation in the color vision of New World monkeys. Many females have trichromatic vision, whereas some females and all males have dichromatic vision. The selective pressures that maintain this polymorphism are unclear. In the present study we compared the performance of dichromats and trichromats in a discrimination task. We examined tri- and dichromatic individuals of two species: brown capuchin monkeys (Cebus apella) and long-tailed macaques (Macaca fascicularis). We also examined one protanomalous chimpanzee (Pan troglodytes). The subjects' task was to discriminate a circular pattern from other patterns in which textural elements differed in orientation and thickness from the background. After they were trained with stimuli of a single color, the subjects were presented with color-camouflaged stimuli with a green/red mosaic overlaid onto the pattern. The dichromatic monkeys and the protanomalous chimpanzee selected the correct stimulus under camouflaged conditions at rates significantly above chance levels, while the trichromats did not. These findings demonstrate that dichromatic nonhuman primates possess a superior visual ability to discriminate color-camouflaged stimuli, and that such an ability may confer selective advantages with respect to the detection of cryptic foods and/or predators.

Color-vision polymorphism in New World monkeys occurs because of an allelic polymorphism of the single-copy red-green middle-to-long-wavelength-sensitive (M/LWS) opsin gene on the X chromosome. Because color-vision types can readily be estimated from allelic types of the M/LWS opsin gene, this polymorphic system offers researchers an excellent opportunity to study the association between vision and behavior. As a prerequisite for such studies, genetically determined color-vision types must be concordant with phenotypes determined directly by behavioral criteria (e.g., by a color discrimination test). However, such correlations between genotypes and phenotypes have been studied only for callitrichine species. Using genetic, electrophysiological, and behavioral approaches, we evaluated the color vision of brown capuchin monkeys (Cebus apella), a representative non-callitrichine model animal for physiology and behavior. Two allelic M/LWS opsins-P545 and P530-were identified in the studied captive population. Females had one or both of the alleles, and males had either one. The retinal sensitivity in P530 dichromats was short-wave shifted relative to that in P545 dichromats, whereas that in P530/P545 trichromats was between the two groups. In a discrimination task using Ishihara pseudo-isochromatic plates, P530/P545 trichromats were successful in discriminating stimuli that P530 and P545 dichromats were unable to discriminate. In a food-search task, P530/P545 trichromats were able to locate red targets among green distracters as quickly as among white distracters, whereas both types of dichromats took longer. These results demonstrate the mutual consistency between genotypes and phenotypes of color vision, and provide a solid genetic basis on which the ecology and evolution of color vision can be investigated.

Primate trichromatic colour vision has been hypothesized to be well tuned for detecting variation in facial coloration, which could be due to selection on either signal wavelengths or the sensitivities of the photoreceptors themselves. We provide one of the first empirical tests of this idea by asking whether, when compared with other visual systems, the information obtained through primate trichromatic vision confers an improved ability to detect the changes in facial colour that female macaque monkeys exhibit when they are proceptive. We presented pairs of digital images of faces of the same monkey to human observers and asked them to select the proceptive face. We tested images that simulated what would be seen by common catarrhine trichromatic vision, two additional trichromatic conditions and three dichromatic conditions. Performance under conditions of common catarrhine trichromacy, and trichromacy with narrowly separated LM cone pigments (common in female platyrrhines), was better than for evenly spaced trichromacy or for any of the dichromatic conditions. These results suggest that primate trichromatic colour vision confers excellent ability to detect meaningful variation in primate face colour. This is consistent with the hypothesis that social information detection has acted on either primate signal spectral reflectance or photoreceptor spectral tuning, or both.

Opsins provide an excellent model system for studying evolutionary interconnections at genetic, phenotypic and behavioural levels. Primates have evolved a unique ability for trichromatic colour vision from a dichromatic mammalian ancestor. This was accomplished via allelic differentiation (e.g. most New World monkeys) or gene duplication (e.g. Old World primates) of the middle to long-wavelength sensitive (M/LWS) opsin gene. However, questions remain regarding the behavioural adaptations of primate trichromacy. Allelic differentiation of the M/LWS opsins results in extensive colour vision variability in New World monkeys, where trichromats and dichromats are found in the same breeding population, enabling us to directly compare visual performances among different colour vision phenotypes. Thus, New World monkeys can serve as an excellent model to understand and evaluate the adaptive significance of primate trichromacy in a behavioural context. In this chapter, we summarise recent findings on colour vision evolution in vertebrates, with special emphasis on primates, and introduce our genetic and behavioural study on primate colour vision polymorphism and adaptation.

Color provides a reliable cue for object detection and identification during various behaviors such as foraging, mate choice, predator avoidance, and navigation. The total number of colors that a visual system can discriminate is largely dependent on the number of different spectral types of cone opsins present in the retina and the spectral separations among them. Thus, opsins provide an excellent model system to study evolutionary interconnections at genetic, phenotypic, and behavioral levels. Primates have evolved a unique ability for three-dimensional color vision (trichromacy) from the two-dimensional color vision (dichromacy) present in the majority of other mammals. This development was accomplished via allelic differentiation (e.g., most New World monkeys) or gene duplication (e.g., Old World primates) of the middle to long wavelength-sensitive (M/LWS, or red–green) opsin gene. However, questions remain regarding the behavioral adaptations of primate trichromacy. Allelic differentiation of the M/LWS opsins results in extensive color vision variability in New World monkeys, where trichromats and dichromats are found in the same breeding population, enabling us to directly compare visual performances among different color vision phenotypes. Thus, New World monkeys can serve as an excellent model to understand and evaluate the adaptive significance of primate trichromacy in a behavioral context. In this chapter, we summarize recent findings on color vision evolution in primates and other vertebrates and introduce our genetic and behavioral study of vision–behavior interrelationships in free-ranging sympatric capuchin and spider monkey populations in Costa Rica.