The Heterozygote Superiority Hypothesis for Polymorphic Color Vision Is Not Supported by Long-Term Fitness Data from Wild Neotropical Monkeys

The leading explanatory model for the widespread occurrence of color vision polymorphism in Neotropical primates is the heterozygote superiority hypothesis, which postulates that trichromatic individuals have a fitness advantage over other phenotypes because redgreen chromatic discrimination is useful for foraging, social signaling, or predator detection. Alternative explanatory models predict that dichromatic and trichromatic phenotypes are each suited to distinct tasks. To conclusively evaluate these models, one must determine whether proposed visual advantages translate into differential fitness of trichromatic and dichromatic individuals. We tested whether color vision phenotype is a significant predictor of female fitness in a population of wild capuchins, using longterm 26 years survival and fertility data. We found no advantage to trichromats over dichromats for three fitness measures fertility rates, offspring survival and maternal survival. This finding suggests that a selective mechanism other than heterozygote advantage is operating to maintain the color vision polymorphism. We propose that attention be directed to field testing the alternative mechanisms of balancing selection proposed to explain opsin polymorphism nichedivergence, frequencydependence and mutual benefit of association. This is the first indepth, longterm study examining the effects of color vision variation on survival and reproductive success in a naturallyoccurring population of primates.     

Molecular evidence for selection on female color polymorphism in the damselfly Ischnura graellsii

The significance of female color polymorphism in Odonata remains controversial despite many field studies. The importance of random factors (founder effects, genetic drift and migration) versus selective forces for the maintenance of this polymorphism is still discussed. In this study, we specifically test whether the female color polymorphism of Ischnura graellsii (Odonata, Coenagrionidae) is under selection in the wild. We compared the degree of genetic differentiation based on RAPD markers (assumed to be neutral) with the degree of differentiation based on color alleles. Weir and Cockerham's theta values showed a significant degree of population differentiation for both sets of loci (RAPD and color alleles) but the estimated degree of population differentiation (theta) was significantly greater for the set of RAPD loci. This result shows that some sort of selection contributes to the maintenance of similar color morph frequencies across the studied populations. Our results combined with those of previous field studies suggest that at least in some I. graellsii populations, density-dependent mechanisms might help to prevent the loss of this polymorphism but cannot explain the similarity in morph frequencies among populations.     

HLA DNA sequence variation among human populations: molecular signatures of demographic and selective events

Molecular differences between HLA alleles vary up to 57 nucleotides within the peptide binding coding region of human Major Histocompatibility Complex (MHC) genes, but it is still unclear whether this variation results from a stochastic process or from selective constraints related to functional differences among HLA molecules. Although HLA alleles are generally treated as equidistant molecular units in population genetic studies, DNA sequence diversity among populations is also crucial to interpret the observed HLA polymorphism. In this study, we used a large dataset of 2,062 DNA sequences defined for the different HLA alleles to analyze nucleotide diversity of seven HLA genes in 23,500 individuals of about 200 populations spread worldwide. We first analyzed the HLA molecular structure and diversity of these populations in relation to geographic variation and we further investigated possible departures from selective neutrality through Tajima's tests and mismatch distributions. All results were compared to those obtained by classical approaches applied to HLA allele frequencies.Our study shows that the global patterns of HLA nucleotide diversity among populations are significantly correlated to geography, although in some specific cases the molecular information reveals unexpected genetic relationships. At all loci except HLA-DPB1, populations have accumulated a high proportion of very divergent alleles, suggesting an advantage of heterozygotes expressing molecularly distant HLA molecules (asymmetric overdominant selection model). However, both different intensities of selection and unequal levels of gene conversion may explain the heterogeneous mismatch distributions observed among the loci. Also, distinctive patterns of sequence divergence observed at the HLA-DPB1 locus suggest current neutrality but old selective pressures on this gene. We conclude that HLA DNA sequences advantageously complement HLA allele frequencies as a source of data used to explore the genetic history of human populations, and that their analysis allows a more thorough investigation of human MHC molecular evolution.     

SELECTION ON THE COLOR POLYMORPHISM IN HAWAIIAN HAPPY-FACE SPIDERS: EVIDENCE FROM GENETIC STRUCTURE AND TEMPORAL FLUCTUATIONS

Throughout this century genetic polymorphisms for color have been widely used as a research tool to allow insights into key evolutionary processes. Although color variants can often be diverse within populations, frequencies of different morphs may be similar across populations, either as a result of balancing selection or gene flow. Under these circumstances selection can be extremely difficult to demonstrate. Here we test for balancing selection on the naturally occurring color forms of the Hawaiian happy-face spider, Theridion grallator with two approaches. First, allozyme loci are used to generate a null model against which to test selection. Frequencies of alleles involved in the color polymorphism of T. grallator are used to generate another estimate for comparison. The results suggest that statistically similar frequencies of color morphs among populations of T. grallator may be maintained by some form of balancing selection. Second, we make use of an unusual event in which the normally stable frequencies of unpatterned and patterned morphs within a population were found to have shifted toward an excess of unpatterned morphs. We scored offspring of all fertilized, unpatterned (bottom-recessive) females found during this period of skewed morph frequencies and also in a year when morph frequencies were normal to deduce paternal color phenotypes. Mating was found to be random in the normal year, but in the perturbed year females had mated with rare (patterned) males twice as frequently as expected on the basis of the frequency of this morph type in the population. Both of these results are consistent with selection operating on the color polymorphism, and we speculate that apostatic selection, perhaps mediated by bird predators, may provide the mechanism.     

Color vision and niche partitioning in a diverse neotropical primate community in lowland Amazonian Ecuador

A recent focus in community ecology has been on how within‐species variability shapes interspecific niche partitioning. Primate color vision offers a rich system in which to explore this issue. Most neotropical primates exhibit intraspecific variation in color vision due to allelic variation at the middle‐to‐long‐wavelength opsin gene on the X chromosome. Studies of opsin polymorphisms have typically sampled primates from different sites, limiting the ability to relate this genetic diversity to niche partitioning. We surveyed genetic variation in color vision of five primate species, belonging to all three families of the primate infraorder Platyrrhini, found in the Yasuní Biosphere Reserve in Ecuador. The frugivorous spider monkeys and woolly monkeys (Ateles belzebuth and Lagothrix lagotricha poeppigii, family Atelidae) each had two opsin alleles, and more than 75% of individuals carried the longest‐wavelength (553–556 nm) allele. Among the other species, Saimiri sciureus macrodon (family Cebidae) and Pithecia aequatorialis (family Pitheciidae) had three alleles, while Plecturocebus discolor (family Pitheciidae) had four alleles—the largest number yet identified in a wild population of titi monkeys. For all three non‐atelid species, the middle‐wavelength (545 nm) allele was the most common. Overall, we identified genetic evidence of fourteen different visual phenotypes—seven types of dichromats and seven trichromats—among the five sympatric taxa. The differences we found suggest that interspecific competition among primates may influence intraspecific frequencies of opsin alleles. The diversity we describe invites detailed study of foraging behavior of different vision phenotypes to learn how they may contribute to niche partitioning.     

Characterization of opsin gene alleles affecting color vision in a wild population of titi monkeys (Callicebus brunneus)

The color vision of most platyrrhine primates is determined by alleles at the polymorphic X-linked locus coding for the opsin responsible for the middle- to long-wavelength (M/L) cone photopigment. Females who are heterozygous at the locus have trichromatic vision, whereas homozygous females and all males are dichromatic. This study characterized the opsin alleles in a wild population of the socially monogamous platyrrhine monkey Callicebus brunneus (the brown titi monkey), a primate that an earlier study suggests may possess an unusual number of alleles at this locus and thus may be a subject of special interest in the study of primate color vision. Direct sequencing of regions of the M/L opsin gene using feces-, blood-, and saliva-derived DNA obtained from 14 individuals yielded evidence for the presence of three functionally distinct alleles, corresponding to the most common M/L photopigment variants inferred from a physiological study of cone spectral sensitivity in captive Callicebus.     

Comparative use of color vision for frugivory by sympatric species of platyrrhines

Ateles spp. and Alouatta spp. are often sympatric, and although they are mainly frugivorous and folivorous, respectively, they consume some of the same fruit species. However, they differ in terms of color vision, which is thought to be important for fruit detection. Alouatta spp. have routine trichromatic color vision, while Ateles spp. presents the classic polymorphism of platyrrhines: heterozygous females have trichromatic color vision, and males and homozygous females have dichromatic vision. Given these perceptual differences, one might expect Alouatta spp. to consume more reddish fruits than Ateles spp., since trichromats have an advantage for detecting fruits of that hue. Furthermore, since Ateles spp. have up to six different color vision phenotypes, as do most other platyrrhines, they might be expected to include fruits with a wider variety of hues in their diet than Alouatta spp. To test these hypotheses we studied the fruit foraging behavior of sympatric Alouatta palliata and Ateles geoffroyi in Costa Rica, and modeled the detectability of fruit via the various color vision phenotypes in these primates. We found little similarity in fruit diet between these two species (Morisita = 0.086). Furthermore, despite its polymorphism, A. geoffroyi consumed more reddish fruits than A. palliata, which consumed more greenish fruits. Our modeling results suggest that most fruit species included in the diet of A. geoffroyi can be discriminated by most color vision phenotypes present in the population. These findings show that the effect of polymorphism in platyrrhines on fruit detection may not be a disadvantage for frugivory. We suggest that routine trichromacy may be advantageous for other foraging tasks, such as feeding on young leaves.     

The Behavioral Ecology of Color Vision: Considering Fruit Conspicuity,Detection Distance and Dietary Importance

Primate color vision is well suited for investigating the genetic basis of foraging behavior owing to a clear genotype–phenotype linkage. Finding fruits amid tropical foliage has long been proffered as an adaptive explanation for primate trichromacy, yet there is a dearth of systematic evaluations of frugivory as an ecological selective force. We studied the behavioral ecology of wild capuchins (Cebus capucinus) in northwestern Costa Rica across the annual cycle and modeled the ability of three dichromatic and three trichromatic phenotypes to discriminate fruits from leaves, a task that represents long-distance search for food patches in a tropical forest. Models of the trichromatic phenotypes could correctly discriminate approximately three-quarters of the total capuchin dietary fruits from leaves, including some fruits subjectively classified as having “cryptic” (greenish-brownish) hues. In contrast, models of dichromatic phenotypes could discriminate fewer than one-third of the fruits. This pattern held when we restricted our analysis to only the most heavily consumed diet items, preferred foods, or seasonally critical species. We in addition highlight the potential of fruit species with small patch sizes to confer an advantage to trichromats, as these resources are anticipated to provide a high finder’s reward. Our results are consistent with the hypothesis that long-distance detection of fruit patches exerts a selective pressure on trichromacy in neotropical primates, and suggest that greenish-brownish fruits might have played an underappreciated role in the evolution of primate color vision.     

Contrasting Mode of Evolution at a Coat Color Locus in Wild and Domestic Pigs

Despite having only begun ~10,000 years ago, the process of domestication has resulted in a degree of phenotypic variation within individual species normally associated with much deeper evolutionary time scales. Though many variable traits found in domestic animals are the result of relatively recent human-mediated selection, uncertainty remains as to whether the modern ubiquity of long-standing variable traits such as coat color results from selection or drift, and whether the underlying alleles were present in the wild ancestor or appeared after domestication began. Here, through an investigation of sequence diversity at the porcine melanocortin receptor 1 (MC1R) locus, we provide evidence that wild and domestic pig (Sus scrofa) haplotypes from China and Europe are the result of strikingly different selection pressures, and that coat color variation is the result of intentional selection for alleles that appeared after the advent of domestication. Asian and European wild boar (evolutionarily distinct subspecies) differed only by synonymous substitutions, demonstrating that camouflage coat color is maintained by purifying selection. In domestic pigs, however, each of nine unique mutations altered the amino acid sequence thus generating coat color diversity. Most domestic MC1R alleles differed by more than one mutation from the wild-type, implying a long history of strong positive selection for coat color variants, during which time humans have cherry-picked rare mutations that would be quickly eliminated in wild contexts. This pattern demonstrates that coat color phenotypes result from direct human selection and not via a simple relaxation of natural selective pressures.     

Frequencies of protan and deutan alleles in some Israeli communities and a note on the selection-relaxation hypothesis

Anomaloscopic diagnoses of red-green vision defects are reported and compared to the Ishihara tests for six Israeli populations. The highest frequencies of defects, about 10%, were found in an Arab sample and among Ashkenazi Jews; the lowest — about 4% — among Yemenite Jews. Heterogeneity was also found regarding the relative frequencies of the different alleles; these differences are due primarily to alleles causing milder defects (particularly deuteranomaly) while frequencies of anopias are rather similar. It seems that the same phenomenon prevails for other population differences as well. These findings are discussed in relation to the hypothesis that present-day high rates of colorblindness in some populations may be explained by the relaxation of selection pressure against colorblindness.     

Considering the Influence of Nonadaptive Evolution on Primate Color Vision

Color vision in primates is variable across species, and it represents a rare trait in which the genetic mechanisms underlying phenotypic variation are fairly well-understood. Research on primate color vision has largely focused on adaptive explanations for observed variation, but it remains unclear why some species have trichromatic or polymorphic color vision while others are red-green color blind. Lemurs, in particular, are highly variable. While some species are polymorphic, many closely-related species are strictly dichromatic. We provide the first characterization of color vision in a wild population of red-bellied lemurs (Eulemur rubriventer, Ranomafana National Park, Madagascar) with a sample size (87 individuals; N_{X chromosomes} = 134) large enough to detect even rare variants (0.95 probability of detection at ≥ 3% frequency). By sequencing exon 5 of the X-linked opsin gene we identified opsin spectral sensitivity based on known diagnostic sites and found this population to be dichromatic and monomorphic for a long wavelength allele. Apparent fixation of this long allele is in contrast to previously published accounts of Eulemur species, which exhibit either polymorphic color vision or only the medium wavelength opsin. This unexpected result may represent loss of color vision variation, which could occur through selective processes and/or genetic drift (e.g., genetic bottleneck). To indirectly assess the latter scenario, we genotyped 55 adult red-bellied lemurs at seven variable microsatellite loci and used heterozygosity excess and M-ratio tests to assess if this population may have experienced a recent genetic bottleneck. Results of heterozygosity excess but not M-ratio tests suggest a bottleneck might have occurred in this red-bellied lemur population. Therefore, while selection may also play a role, the unique color vision observed in this population might have been influenced by a recent genetic bottleneck. These results emphasize the need to consider adaptive and nonadaptive mechanisms of color vision evolution in primates.     

Molecular Markers Allow to Remove Introgressed Genetic Background: A Simulation Study

The maintenance of genetically differentiated populations can be important for several reasons (whether for wild species or domestic breeds of economic interest). When those populations are introgressed by foreign individuals, methods to eliminate the exogenous alleles can be implemented to recover the native genetic background. This study used computer simulations to explore the usefulness of several molecular based diagnostic approaches to recover of a native population after suffering an introgression event where some exogenous alleles were admixed for a few generations. To remove the exogenous alleles, different types of molecular markers were used in order to decide which of the available individuals contributed descendants to next generation and their number of offspring. Recovery was most efficient using diagnostic markers (i.e., with private alleles) and least efficient when using alleles present in both native and exogenous populations at different frequencies. The increased inbreeding was a side-effect of the management strategy. Both values (% of native alleles and inbreeding) were largely dependent on the amount of exogenous individuals entering the population and the number of generations of admixture that occurred prior to management.     

Sugar concentration of fruits and their detection via color in the Central American spider monkey (Ateles geoffroyi)

Although most arguments explaining the predominance of polymorphic color vision in platyrrhine monkeys are linked to the advantage of trichromacy over dichromacy for foraging for ripe fruits, little information exists on the relationship between nutritional reward and performance in fruit detection with different types of color vision. The principal reward of most fruits is sugar, and thus it seems logical to investigate whether fruit coloration provides a long-distance sensory cue to primates that correlates with sugar content. Here we test the hypothesis that fruit detection performance via trichromatic color vision phenotypes provides better information regarding sugar concentration than dichromatic phenotypes (i.e., is a color vision phenotype with sufficient red-green (RG) differentiation necessary to "reveal" the concentration of major sugars in fruits?). Accordingly, we studied the fruit foraging behavior of Ateles geoffroyi by measuring both the reflectance spectra and the concentrations of major sugars in the consumed fruits. We modeled detection performance with different color phenotypes. Our results provide some support for the hypothesis. The yellow-blue (YB) color signal, which is the only one available to dichromats, was not significantly related to sugar concentration. The RG color vision signal, which is present only in trichromats, was significantly correlated with sugar content, but only when the latter was defined by glucose. There was in fact a consistent negative relationship between fruit detection performance and sucrose concentration, although this was not significant for the 430 nm and 550 nm phenotypes. The regular trichromatic phenotypes (430 nm, 533 nm, and 565 nm) showed higher correlations between fruit performance and glucose concentration than the other two trichromatic phenotypes. Our study documents a trichromatic foraging advantage in terms of fruit quality, and suggests that trichromatic color vision is advantageous over dichromatic color vision for detecting sugar-rich fruits.     

Born blonde: a recessive loss‐of‐function mutation in the melanocortin 1 receptor is associated with cream coat coloration in Antarctic fur seals

Although the genetic basis of color variation has been extensively studied in humans and domestic animals, the genetic polymorphisms responsible for different color morphs remain to be elucidated in many wild vertebrate species. For example, hypopigmentation has been observed in numerous marine mammal species but the underlying mutations have not been identified. A particularly compelling candidate gene for explaining color polymorphism is the melanocortin 1 receptor (MC1R), which plays a key role in the regulation of pigment production. We therefore used Antarctic fur seals (Arctocephalus gazella) as a highly tractable marine mammal system with which to test for an association between nucleotide variation at the MC1R and melanin‐based coat color phenotypes. By sequencing 70 wild‐type individuals with dark‐colored coats and 26 hypopigmented individuals with cream‐colored coats, we identified a nonsynonymous mutation that results in the substitution of serine with phenylalanine at an evolutionarily highly conserved structural domain. All of the hypopigmented individuals were homozygous for the allele coding for phenylalanine, consistent with a recessive loss‐of‐function allele. In order to test for cryptic population structure, which can generate artefactual associations, and to evaluate whether homozygosity at the MC1R could be indicative of low genome‐wide heterozygosity, we also genotyped all of the individuals at 50 polymorphic microsatellite loci. We were unable to detect any population structure and also found that wild‐type and hypopigmented individuals did not differ significantly in their standardized multilocus heterozygosity. Such a lack of association implies that hypopigmented individuals are unlikely to suffer disproportionately from inbreeding depression, and hence, we have no reason to believe that they are at a selective disadvantage in the wider population.     

Maternal Inheritance of Enzymes in the Mealybug PSEUDOCOCCUS OBSCURUS (Homoptera)

In the mealybug Pseudococcus obscurus Essig (Pseudococcidae) two esterases, a tyrosinase and a mannosephosphate isomerase, exhibited an unusual type of maternal inheritance. Electromorphs (alleles) were transmitted by both parent but segregation was delayed by one generation and full sisters always had the same phenotype. Moreover, for esterase-1, in which three alleles were present, some of the females exhibited all three alleles. Several other polymorphic loci exhibited normal transmission and segregation. This mode of inheritance can be readily explained by assuming that most or all of the enzymes coded for by these loci are produced by the mycetocytes. The mycetocytes house intracellular bacteria-like symbionts and are usually formed by the fusion ofthe polar bodies and one or more cleavage nuclei. For a locus with two alleles exhibiting this type of inheritance, the expected frequencies of the three phenotypes are p3, 3pq an equation is presented for estimating the frequency of alleles from the frequencies of the phenotypes and it is shown that for three samples from wild populations there is a good agreement between the expected and observed frequencies of the phenotypes.     

Enzyme polymorphisms in the European oyster, Ostrea edulis L.

Extracts of the digestive diverticula of more than 300 individuals from four geographically separated populations of the European oyster, Ostrea edulis L. have been examined by electrophoresis for esterase and phosphoglucose isomerase polymorphisms. Three regions of esterase variability have been detected in the electrophoretograms. It is inferred that the variants in two of these regions are governed by two co-dominant alleles at each of two loci. Two phenotypes of phosphoglucose isomerase, which is inferred to be a dimeric enzyme encoded by two alleles at a single locus, have been observed. Allele frequencies and phenotype distributions are compared in the four populations. It is concluded that the populations differ genetically at the loci investigated, the magnitude of the differences being generally greatest between different 'physiological races'.     

Isoallele Frequencies in Very Large Populations

The frequencies of electrophoretically distinguishable allelic forms of enzymes may be very different from the corresponding frequencies of structurally distinct forms, because many sequence variants may have identical electrophoretic charge. In large populations such frequencies will be determined largely by the number of amino acid sites that are free to vary. The number of distinguishable electrophoretic variants will remain fairly small. Beyond some limiting size, no further effect of population size on allele frequencies is expected, so isolated large populations will have closely similar allele frequencies if polymorphism is due largely to mutation and drift. The most common electrophoretic alleles are expected to be flanked by the next most common, with the rarer alleles increasingly distal. Neither strong selection nor mutation/drift interpretations of enzyme polymorphism are yet disproven, nor is any point between these extremes.     

Type 2 diabetes risk alleles demonstrate extreme directional differentiation among human populations, compared to other diseases

Many disease-susceptible SNPs exhibit significant disparity in ancestral and derived allele frequencies across worldwide populations. While previous studies have examined population differentiation of alleles at specific SNPs, global ethnic patterns of ensembles of disease risk alleles across human diseases are unexamined. To examine these patterns, we manually curated ethnic disease association data from 5,065 papers on human genetic studies representing 1,495 diseases, recording the precise risk alleles and their measured population frequencies and estimated effect sizes. We systematically compared the population frequencies of cross-ethnic risk alleles for each disease across 1,397 individuals from 11 HapMap populations, 1,064 individuals from 53 HGDP populations, and 49 individuals with whole-genome sequences from 10 populations. Type 2 diabetes (T2D) demonstrated extreme directional differentiation of risk allele frequencies across human populations, compared with null distributions of European-frequency matched control genomic alleles and risk alleles for other diseases. Most T2D risk alleles share a consistent pattern of decreasing frequencies along human migration into East Asia. Furthermore, we show that these patterns contribute to disparities in predicted genetic risk across 1,397 HapMap individuals, T2D genetic risk being consistently higher for individuals in the African populations and lower in the Asian populations, irrespective of the ethnicity considered in the initial discovery of risk alleles. We observed a similar pattern in the distribution of T2D Genetic Risk Scores, which are associated with an increased risk of developing diabetes in the Diabetes Prevention Program cohort, for the same individuals. This disparity may be attributable to the promotion of energy storage and usage appropriate to environments and inconsistent energy intake. Our results indicate that the differential frequencies of T2D risk alleles may contribute to the observed disparity in T2D incidence rates across ethnic populations.     

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.     

Color Vision Variation and Foraging Behavior in Wild Neotropical Titi Monkeys (<Emphasis Type="Italic">Callicebus brunneus</Emphasis>): 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.