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In many species the face mediates social communication, conveying meaningful information to other individuals. The face is thus a highly important visual stimulus, and many factors are involved in recognizing individuals from facial information. Capuchin monkeys are excellent subjects for studying facial recognition from a comparative perspective because of their intelligence and their highly social nature. Furthermore, they show polymorphic color vision, with groups containing both dichromatic and trichromatic individuals, which provides an opportunity to examine potential effects of color on facial recognition. In this chapter, I describe experimental research on the relationships between color vision and detection of face color modulations in capuchin monkeys. Using face images of familiar individuals, the color of either the left eye, the right eye, or the nose was shifted in a red or blue direction. Face orientation (upright and inverted) and face identity were also manipulated. Trichromatic monkeys showed no greater sensitivity to face color modulation, but face parts, orientation, and identity all affect their accuracy and reaction times in the detection task. These results indicate that facial stimuli appear equally salient to dichromatic and trichromatic individuals, and that social factors such as dominance and kinship affect face processing in capuchin monkeys.

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.

Realistic appearance and complexity in the visual field are known to affect the strength of vection (visually induced self-motion perception). Although surface properties of materials are, therefore, expected to be visual features that influence vection, to date, the results have been mixed. Here, we used computer graphics to simulate self-motion through rendered 3D tunnels constructed from nine different materials (bark, ceramic, fabric, fur, glass, leather, metal, stone, and wood). There are three ways in which the new stimuli are changed from those found in previous studies: (1) as they move, their appearances interactively change with the 3D structures of the simulated world, as do all the lighting effects and 3D geometric appearances, (2) they are colored, (3) and their components covered a large portion of the visual field. The entire inner surface of each tunnel was composed from one of the nine materials, and optic flow was evoked when an observer virtually moved through the tunnel. Bark, fabric, leather, stone, and wood effectively induced strong vection, whereas, ceramic, glass, fur, and metal did not. Regression analyses suggested that low-level image features such as the lighting and amplitude of spatial frequency were the main factors that modulated vection strength. Additionally, subjective impressions of the nine surface materials showed that the perceived depth, smoothness, and rigidity were related to the perceived vection strength. Overall, our results indicate that surface properties of materials do indeed modulate vection strength.

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.

Visually identifying and categorizing the material composition of objects before actually interacting with them is an important skill for operating smoothly and safely in the world. This ability is assumed to have been shaped by evolution; therefore, non-human animals should share similar categorization abilities. Little is known, however, about how non-human animals do this. We tested whether tufted capuchin monkeys (Cebus apella) were able to visually categorize images that represented nine different materials (metal, ceramic, glass, stone, bark, wood, leather, fabric, and fur), and we compared their performance with that of humans. Capuchins showed excellent categorization abilities for images of fur, which is a familiar material to captive monkeys. Humans showed a tendency to confuse material categories that resembled each other visually and/or semantically. Correlation analyses on reaction time showed that both species made correct choices rapidly in selecting glossy categories like metal and ceramic compared with matte categories like fabric and stone, which contain minute patterns. Overall, our results suggest that monkeys share similar perceptual tendencies with humans in visual categorization of material images to some extent and the potential to categorize materials frequently encountered in their daily lives by visual observation.

Eye tracking can be used for eye-gaze-based authentication in public settings, such as for registration on personal computers and automated teller machines. In this study, we conducted a series of measurements with low-cost eyetracking devices to assess the feasibility of their use in such settings. We investigated the devices' minimum and maximum viewing distance limits as well as viewing angle range. Both these parameters were tested under three different lighting conditions. The eye-tracking devices used in the measurements were among the most cost-effective devices commercially available today (Tobii EyeX© and Eye Tribe©). The results showed that the minimum and maximum viewing limit of the Tobii EyeX© did not vary significantly with different lighting conditions, and neither did the viewing angle range. The maximum viewing distance of the Eye Tribe© was significantly different between two conditions of artificial lighting, although the average difference was just 1 cm. The lowest viewing angle that allowed registration into the Eye Tribe© system also differed significantly between the two artificial lighting conditions, but here too the average angle difference was small (0.63°). Taken together, the results show that the performance of the two low- cost eye trackers tested here is robust enough under different conditions of illuminance and luminance for registration into the system.

It is known that the use of glasses can hamper the quality and speed of user registration into eye-tracking devices. Studies have been done in which the performances of various eye-tracking devices were compared, typically under ideal viewing angles, with the user sitting behind a display under a fixed lighting condition. Here we investigated the influence of the use of glasses on the quality and time of user registration into a low-cost eye-tracking device under various lighting conditions. Furthermore, we compared the use of glasses on registration within the same group of participants. Participants with prescription glasses were asked to register into the eye-tracking device both with and without their glasses, if possible, and users without prescription glasses or with contact lenses were also asked to register without glasses or with replica, nonprescription glasses. The present results showed indeed that the use of glasses negatively influenced registration quality and time — significantly here, however, only when registration was performed under artificial lighting. Under natural lighting, the difference in registration quality and speed did not reach significance, but bordered on significance. A follow-up measurement confirmed these results, and suggested that calibration with glasses can improve when participants register under ‘ideal’ viewing angles for their particular viewing position.

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.

Every object in the world has its own surface quality that is a reflection of the material from which the object is made. We can easily identify and categorize materials (wood, metal, fabric etc.) at a glance, and this ability enables us to decide how to interact appropriately with these objects. Little is known, however, about how materials are represented in the brain, or how that representation is related to material perception or the physical properties of material surface. By combining multivoxel pattern analysis of functional magnetic resonance imaging data with perceptual and image-based physical measures of material properties, we found that the way visual information about materials is coded gradually changes from an image-based representation in early visual areas to a perceptual representation in the ventral higher-order visual areas. We suggest that meaningful information about multimodal aspects of real-world materials reside in the ventral cortex around the fusiform gyrus, where it can be utilized for categorization of materials.

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.

The colour vision polymorphism of New World monkeys results from allelic variations of the middle-to-long-wave-sensitive (M/LWS) visual pigments. On the basis of sequence comparison, spectral differences among the alleles have been ascribed to amino acid residues at sites 180, 229, 233, 277, and 285. While the significant spectral effects have been demonstrated for sites 180, 277, and 285 by site-directed mutagenesis for a large number of vertebrate M/LWS pigments (the "three-site rule"), effects at sites 229 and 233 remain untested. Here we measured absorption spectra of the reconstituted M/LWS pigments from the tri-allelic squirrel monkey (Saimiri sciureus) and the mono-allelic owl monkey (Aotus trivirgatus). The peak absorption spectra (lambdamax) of Saimiri pigments were 532, 545, and 558 nm and that of Aotus pigment 539 nm, being consistent with the prediction from the three-site rule. Our site-directed mutagenesis for sites 229 and 233 showed that their mutational effects for lambdamax values were negligible. These results preclude the necessity of examining exon 4, encoding the residues at sites 229 and 233, of M/LWS pigment genes for colour-vision typing of New World monkeys.

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.

This work was supported by the National Evolutionary Synthesis Center (NESCent) through support of a working group led by C.L.N. and B.H. NESCent is supported by the National Science Foundation (NSF) EF-0905606. For training in phylogenetic comparative methods, we thank the AnthroTree Workshop (supported by NSF BCS-0923791). Y.S. thanks the National Natural Science Foundation of China (Project 31170995) and National Basic Research Program (973 Program: 2010CB833904). E.E.B. thanks the Duke Vertical Integration Program and the Duke Undergraduate Research Support Office. J.M.P. was supported by a Newton International Fellowship from the Royal Society and the British Academy. L.R.S. thanks the James S. McDonnell Foundation for Award 220020242. L.J.N.B. and M.L.P. acknowledge the National Institutes of Mental Health (R01-MH096875 and R01-MH089484), a Duke Institute for Brain Sciences Incubator Award (to M.L.P.), and a Duke Center for Interdisciplinary Decision Sciences Fellowship (to L.J.N.B.). E.V. and E.A. thank the Programma Nazionale per la Ricerca–Consiglio Nazionale delle Ricerche (CNR) Aging Program 2012–2014 for financial support, Roma Capitale–Museo Civico di Zoologia and Fondazione Bioparco for hosting the Istituto di Scienze e Tecnologie della Cognizione–CNR Unit of Cognitive Primatology and Primate Centre, and Massimiliano Bianchi and Simone Catarinacci for assistance with capuchin monkeys. K.F. thanks the Japan Society for the Promotion of Science (JSPS) for Grant-in-Aid for Scientific Research 20220004. F. Aureli thanks the Stages in the Evolution and Development of Sign Use project (Contract 012-984 NESTPathfinder) and the Integrating Cooperation Research Across Europe project (Contract 043318), both funded by the European Community’s Sixth Framework Programme (FP6/2002–2006). F. Amici was supported by Humboldt Research Fellowship for Postdoctoral Researchers (Humboldt ID 1138999). L.F.J. and M.M.D. acknowledge NSF Electrical, Communications, and Cyber Systems Grant 1028319 (to L.F.J.) and an NSF Graduate Fellowship (to M.M.D.). C.H. thanks Grant-in-Aid for JSPS Fellows (10J04395). A.T. thanks Research Fellowships of the JSPS for Young Scientists (21264). F.R. and Z.V. acknowledge Austrian Science Fund (FWF) Project P21244-B17, the European Research Council (ERC) under the European Union’s Seventh Framework Programme (FP/2007–2013)/ERC Grant Agreement 311870 (to F.R.), Vienna Science and Technology Fund Project CS11-026 (to Z.V.), and many private sponsors, including Royal Canin for financial support and the Game Park Ernstbrunn for hosting the Wolf Science Center. S.M.R. thanks the Natural Sciences and Engineering Research Council (Canada). J.K.Y. thanks the US Department of Agriculture–Wildlife Services–National Wildlife Research Center. J.F.C. thanks the James S. McDonnell Foundation and Alfred P. Sloan Foundation. E.L.M. and B.H. thank the Duke Lemur Center and acknowledge National Institutes of Health Grant 5 R03 HD070649-02 and NSF Grants DGE-1106401, NSF-BCS-27552, and NSF-BCS-25172. This is Publication 1265 of the Duke Lemur Center. Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution. Postprint

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.

The X-chromosomal locality of the red-green-sensitive opsin genes has been the norm for all mammals and is essential for color vision of higher primates. Owl monkeys (Aotus), a genus of New World monkeys, are the only nocturnal higher primates and are severely color-blind. We demonstrate that the owl monkeys possess extra red-green opsin genes on the Y-chromosome. The Y-linked opsin genes were found to be extremely varied, in one male appearing to be a functional gene and in other males to be multicopy pseudogenes. These Y-linked opsin genes should offer a rare opportunity to study the evolutionary fate of genes translocated to the Y chromosome.

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.

Color vision is an important characteristic of primates and, intriguingly, Neotropical monkeys are highly polymorphic for this trait. Recent field studies have challenged the conventional view that trichromatic color vision is more adaptive than dichromatic color vision. No study has investigated the pattern of genetic variation in the long to middle wavelength‐ sensitive (L-M or red‐green) opsin gene as compared with that of other genomic regions (neutral references) in wild populations of New World monkeys to look for the signature of natural selection. Here, we report such a study conducted on spider monkeys and capuchin monkeys inhabiting Santa Rosa National Park, Costa Rica. The nucleotide sequence of the L-M opsin gene was more polymorphic than the sequences of the neutral references, although the opsin-gene sequences were not more divergent between the two species than were the sequences of the neutral references. In a coalescence simulation that took into account the observed nucleotide diversity of the neutral references, the Tajima’s D value of the L-M opsin gene deviated significantly in a positive direction from the expected range. These results are the first to statistically demonstrate balancing selection acting on the polymorphic L-M opsin gene of New World monkeys. Taking the results of behavioral and genetic studies together, the balancing selection we detected may indicate that coexistence of different color-vision types in the same population, also characteristic of humans, is adaptive.

Trichromatic primates have a 'red-green' chromatic channel in addition to luminance and 'blue-yellow' channels. It has been argued that the red-green channel evolved in primates as an adaptation for detecting reddish or yellowish objects, such as ripe fruits, against a background of foliage. However, foraging advantages to trichromatic primates remain unverified by behavioral observation of primates in their natural habitats. New World monkeys (platyrrhines) are an excellent model for this evaluation because of the highly polymorphic nature of their color vision due to allelic variation of the L-M opsin gene on the X chromosome. In this study we carried out field observations of a group of wild, frugivorous black-handed spider monkeys (Ateles geoffroyi frontatus, Gray 1842, Platyrrhini), consisting of both dichromats (n = 12) and trichromats (n = 9) in Santa Rosa National Park, Costa Rica. We determined the color vision types of individuals in this group by genotyping their L-M opsin and measured foraging efficiency of each individual for fruits located at a grasping distance. Contrary to the predicted advantage for trichromats, there was no significant difference between dichromats and trichromats in foraging efficiency and we found that the luminance contrast was the main determinant of the variation of foraging efficiency among red-green, blue-yellow and luminance contrasts. Our results suggest that luminance contrast can serve as an important cue in short-range foraging attempts despite other sensory cues that could be available. Additionally, the advantage of red-green color vision in primates may not be as salient as previously thought and needs to be evaluated in further field observations.

The X-chromosomal locality of the red-green-sensitive opsin genes has been the norm for all mammals and is essential for color vision of higher primates. Owl monkeys (Aotus), a genus of New World monkeys, are the only nocturnal higher primates and are severely color-blind. We demonstrate that the owl monkeys possess extra red-green opsin genes on the Y-chromosome. The Y-linked opsin genes were found to be extremely varied, in one male appearing to be a functional gene and in other males to be multicopy pseudogenes. These Y-linked opsin genes should offer a rare opportunity to study the evolutionary fate of genes translocated to the Y chromosome.