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.     

A receiver bias in the origin of three-spined stickleback mate choice

Receiver-bias models of signal evolution predict that male sexually selected traits evolve through prior selection for other functions. Female three-spined sticklebacks (Gasterosteus aculeatus) in many populations show a mating preference for males with a red throat and jaw. It has been proposed that this preference evolved because the choice of males with red coloration confers direct and indirect benefits to females in accordance with the Fisher-Zahavi model of sexual selection. We present indirect evidence that the preference is an effect of a receiver bias in the perceptual or cognitive system of G. aculeatus for the colour red, which may have arisen in the context of foraging. In laboratory trials, male and female three-spined and nine-spined sticklebacks (Pungitius pungitius) responded most strongly to red objects outside a mating context. This result demonstrates a correlation between a sexually selected trait and an intrinsic attraction to red objects, and supports the sensory-exploitation model for the evolution of red nuptial coloration in three-spined sticklebacks.     

Color vision of ancestral organisms of higher primates

The color vision of mammals is controlled by photosensitive proteins called opsins. Most mammals have dichromatic color vision, but hominoids and Old World (OW) monkeys enjoy trichromatic vision, having the blue-, green-, and red-sensitive opsin genes. Most New World (NW) monkeys are either dichromatic or trichromatic, depending on the sex and genotype. Trichromacy in higher primates is believed to have evolved to facilitate the detection of yellow and red fruits against dappled foliage, but the process of evolutionary change from dichromacy to trichromacy is not well understood. Using the parsimony and the newly developed Bayesian methods, we inferred the amino acid sequences of opsins of ancestral organisms of higher primates. The results suggest that the ancestors of OW and NW monkeys lacked the green gene and that the green gene later evolved from the red gene. The fact that the red/green opsin gene has survived the long nocturnal stage of mammalian evolution and that it is under strong purifying selection in organisms that live in dark environments suggests that this gene has another important function in addition to color vision, probably the control of circadian rhythms.      

Evolution and function of routine trichromatic vision in primates

Evolution of the red-green visual subsystem in trichromatic primates has been linked to foraging advantages, namely the detection of either ripe fruits or young leaves amid mature foliage. We tested competing hypotheses globally for eight primate taxa: five with routine trichromatic vision, three without. Routinely trichromatic species ingested leaves that were "red shifted" compared to background foliage more frequently than species lacking this trait. Observed choices were not the reddest possible, suggesting a preference for optimal nutritive gain. There were no similar differences for fruits although red-greenness may sometimes be important in close-range fruit selection. These results suggest that routine trichromacy evolved in a context in which leaf consumption was critical.     

Genetic evidence for the coexistence of pheromone perception and full trichromatic vision in howler monkeys

Vertebrate pheromones are water-soluble chemicals perceived mainly by the vomeronasal organ (VNO) for intraspecific communications. Humans, apes, and Old World (OW) monkeys lack functional genes responsible for the pheromone signal transduction and are generally insensitive to vomeronasal pheromones. It has been hypothesized that the evolutionary deterioration of pheromone sensitivity occurred because pheromone communication became redundant after the emergence of full trichromatic color vision via the duplication of the X-chromosome-linked red/green opsin gene in the common ancestor of hominoids and OW monkeys. Interestingly, full trichromacy also evolved in the New World (NW) howler monkeys via an independent duplication of the same gene. Here we sequenced from three species of howler monkeys an essential component of the VNO pheromone transduction pathway, the gene encoding the ion channel TRP2. In contrast to those of hominoids and OW monkeys, the howler TRP2 sequences have none of the characteristics of pseudogenes. This and other observations indicate that howler monkeys have maintained both their systems of pheromone communication and full trichromatic vision, suggesting that the presence of full trichromacy alone does not lead to the loss of pheromone communication. We suggest that the ecological differences between OW and NW primates, particularly in habitat selection, may have also affected the evolution of pheromone perception.     

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.     

Fruits, foliage and the evolution of primate colour vision

Primates are apparently unique amongst the mammals in possessing trichromatic colour vision. However, not all primates are trichromatic. Amongst the haplorhine (higher) primates, the catarrhines possess uniformly trichromatic colour vision, whereas most of the platyrrhine species exhibit polymorphic colour vision, with a variety of dichromatic and trichromatic phenotypes within the population. It has been suggested that trichromacy in primates and the reflectance functions of certain tropical fruits are aspects of a coevolved seed-dispersal system: primate colour vision has been shaped by the need to find coloured fruits amongst foliage, and the fruits themselves have evolved to be salient to primates and so secure dissemination of their seeds. We review the evidence for and against this hypothesis and we report an empirical test: we show that the spectral positioning of the cone pigments found in trichromatic South American primates is well matched to the task of detecting fruits against a background of leaves. We further report that particular trichromatic platyrrhine phenotypes may be better suited than others to foraging for particular fruits under particular conditions of illumination; and we discuss possible explanations for the maintenance of polymorphic colour vision amongst the platyrrhines.     

Primate Fruit Color: Useful Concept or Alluring Myth?

While the importance of frugivorous primates as seed dispersers is well established, the question of the extent to which they exert selective pressure on fruit color phenotypes is contested. Numerous studies have identified suites of primate fruit colors, but the lack of agreement among them illustrates the difficulty of identifying the match between primate foraging behavior and the extent of primate–plant coevolution. This may indicate that primates do not shape fruit traits, at least in a consistent direction, or that the evolution of fruit color is affected by a complex array of selection pressures in which primates play only a part. Here, we review the role of primates in shaping fruit color in the context of primate color vision phenotypes, and fruit phenotypic constraints and selective pressures. To test the hypothesis that fruit color is subjected to selection pressures by primates, we offer six testable predictions aimed at disentangling the complex array of factors that can contribute to fruit color phenotypes, including animal mutualists, animal antagonists, and developmental and phylogenetic constraints of fruits. We conclude that identifying the importance of primate seed dispersers in shaping fruit visual traits is possible, but more complex than previously thought.     

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.     

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.     

Platyrrhine color signals: New horizons to pursue

Like catarrhines, some platyrrhines show exposed and reddish skin, raising the possibility that reddish signals have evolved convergently. This variation in skin exposure and color combined with sex‐linked polymorphic color vision in platyrrhines presents a unique, and yet underexplored, opportunity to investigate the relative importance of chromatic versus achromatic signals, the influence of color perception on signal evolution, and to understand primate communication broadly. By coding the facial skin exposure and color of 96 platyrrhines, 28 catarrhines, 7 strepsirrhines, 1 tarsiiform, and 13 nonprimates, and by simulating the ancestral character states for these traits, we provide the first analysis of the distribution and evolution of facial skin exposure and color in platyrrhini. We highlight ways in which studying the presence and use of color signals by platyrrhines and other primates will enhance our understanding of the evolution of color signals, and the forces shaping color vision.     

Historical contingency in the evolution of primate color vision

Primates are unique among eutherian mammals for possessing three types of retinal cone. Curiously, catarrhines, platyrrhines, and strepsirhines share this anatomy to different extents, and no hypothesis has hitherto accounted for this variability. Here we propose that the historical biogeography of figs and arborescent palms accounts for the global variation in primate color vision. Specifically, we suggest that primates invaded Paleogene forests characterized by figs and palms, the fruits of which played a keystone function. Primates not only relied on such resources, but also provided high-quality seed dispersal. In turn, figs and palms lost or simply did not evolve conspicuous coloration, as this conferred little advantage for attracting mammals. We suggest that the abundance and coloration of figs and palms offered a selective advantage to foraging groups with mixed capabilities for chromatic distinction. Climatic cooling at the end of the Eocene and into the Neogene resulted in widespread regional extinction or decimation of palms and (probably) figs. In regions where figs and palms became scarce, we suggest primates evolved routine trichromatic vision in order to exploit proteinaceous young leaves as a replacement resource. A survey of the hue and biogeography of extant figs and palms provides some empirical support. Where these resources are infrequent, primates are routinely trichromatic and consume young leaves during seasonal periods of fruit dearth. These results imply a link between the differential evolution of primate color vision and climatic changes during the Eocene-Oligocene transition.     

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

New World monkeys exhibit a color vision polymorphism. It resultsfrom allelic variation of the single-locus middle-to-long wavelengthopsin gene on the X chromosome. Females that are heterozygousfor the gene possess trichromatic vision. All other individualspossess dichromatic vision. The prevailing hypothesis for themaintenance of the color vision polymorphism is through a consistentfitness advantage to heterozygous trichromatic females. Suchfemales are predicted to be more efficient than dichromats whendetecting and selecting fruit. Recent experiments with captivecallitrichid primates provided support for this hypothesis bydemonstrating that color vision phenotype affects behavioralresponses to contrived food targets. Yet, the assumptions thattrichromatic females acquire more calories from fruit, or thatnumber of offspring is linked to caloric intake, remain untested.Here, we assess if, in the wild, heterozygous trichromatic individualsin a group of white-faced capuchins (Cebus capucinus) enjoyan energetic advantage over dichromats when foraging on fruit.Contrary to the assumptions of previous theoretical and experimentalstudies, our analysis of C. capucinus foraging behavior showsthat trichromats do not differ from dichromats in their fruitor energy acquisition rates. For white-faced capuchins, theadvantage of trichromatic vision may be related to the detectionof predators, animal prey, or fruit under mesopic conditions.This result demonstrates the importance of using a fitness currencythat is relevant to individual animals to test evolutionaryhypotheses.     

Preferences for coloured bower decorations can be explained in a nonsexual context

The sensory bias model of sexual selection suggests that elaborate male secondary sexual traits evolved to exploit biases in the female's sensory system. Such biases may have evolved in a nonsexual context. Male bowerbirds build and decorate elaborate structures, bowers, which function as targets of female choice. The colour of decorations used on bowers appears to be important in determining a male's mating success. We tested two predictions made by the sensory bias model, using cache presentation experiments of artificially coloured grapes made to captive bowerbirds of five species. We first searched for evidence of ancestral biases for certain colours that could explain current colour preferences across species. We found no single parsimonious explanation for ancestral patterns of colour preference across the family. We next tested whether female preference patterns could be explained in a nonsexual, foraging, context. For both of the species where sufficient data could be collected, female foraging preferences for grapes were significantly related to male preferences for grapes used as bower decorations. Our results suggest that choice of bower decoration colour may have evolved to exploit a bias in the female's sensory system, originally shaped by selection on foraging practices. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Parallel evolution of sexual isolation in sticklebacks

Mechanisms of speciation are not well understood, despite decades of study. Recent work has focused on how natural and sexual selection cause sexual isolation. Here, we investigate the roles of divergent natural and sexual selection in the evolution of sexual isolation between sympatric species of threespine sticklebacks. We test the importance of morphological and behavioral traits in conferring sexual isolation and examine to what extent these traits have diverged in parallel between multiple, independently evolved species pairs. We use the patterns of evolution in ecological and mating traits to infer the likely nature of selection on sexual isolation. Strong parallel evolution implicates ecologically based divergent natural and/or sexual selection, whereas arbitrary directionality implicates nonecological sexual selection or drift. In multiple pairs we find that sexual isolation arises in the same way: assortative mating on body size and asymmetric isolation due to male nuptial color. Body size and color have diverged in a strongly parallel manner, similar to ecological traits. The data implicate ecologically based divergent natural and sexual selection as engines of speciation in this group.     

Carotenoid availability affects the development of a colour-based mate preference and the sensory bias to which it is genetically linked

Regardless of their origins, mate preferences should, in theory, be shaped by their benefits in a mating context. Here we show that the female preference for carotenoid colouration in guppies (Poecilia reticulata) exhibits a phenotypically plastic response to carotenoid availability, confirming a key prediction of sexual selection theory. Earlier work indicated that this mate preference is genetically linked to, and may be derived from, a sensory bias that occurs in both sexes: attraction to orange objects. The original function of this sensory bias is unknown, but it may help guppies find orange-coloured fruits in the rainforest streams of Trinidad. We show that the sensory bias also exhibits a phenotypically plastic response to carotenoid availability, but only in females. The sex-specificity of this reaction norm argues against the hypothesis that it evolved in a foraging context. We infer instead that the sensory bias has been modified as a correlated effect of selection on the mate preference. These results provide a new type of support for the hypothesis that mate preferences for sexual characters evolve in response to the benefits of mate choice--the alternatives being that such preferences evolve entirely in a non-mating context or in response to the costs of mating.     

Innate and Learned Colour Preference in the Zebrafish, Danio rerio

Receiver biases towards specific sensory signals have been demonstrated in insects, birds and fish, both in the context of foraging and mate choice. In some cases, signals important in sexual selection appear to have evolved by exploiting a pre-existing bias in the sensory system. For instance, female preferences for male nuptial colouration may have arisen from selection on foraging practices. Using the zebrafish ( Danio rerio ), a species in which red is not a factor in mate choice, we tested for a foraging bias towards the colour red. We further investigated the plasticity of foraging biases by raising groups of fish on diets consisting solely of red, blue, green or white food. When we subsequently tested their colour preferences in a foraging context, each group responded most strongly to red, irrespective of the colour of food with which they had been conditioned. We also detected a significant effect of conditioning on colour preferences; fish responded more strongly to the colour that matched diet colour than to other colours. The observed receiver bias towards red may have evolved as an adaptive preference for carotenoid compounds in their diet. While the bias to red appears to be innate, our results indicate that learning is also important in shaping foraging biases.     

A TEST OF THE CRITICAL ASSUMPTION OF THE SENSORY BIAS MODEL FOR THE EVOLUTION OF FEMALE MATING PREFERENCE USING NEURAL NETWORKS

The sensory bias model for the evolution of mating preferences states that mating preferences evolve as correlated responses to selection on nonmating behaviors sharing a common sensory system. The critical assumption is that pleiotropy creates genetic correlations that affect the response to selection. I simulated selection on populations of neural networks to test this. First, I selected for various combinations of foraging and mating preferences. Sensory bias predicts that populations with preferences for like-colored objects (red food and red mates) should evolve more readily than preferences for differently colored objects (red food and blue mates). Here, I found no evidence for sensory bias. The responses to selection on foraging and mating preferences were independent of one another. Second, I selected on foraging preferences alone and asked whether there were correlated responses for increased mating preferences for like-colored mates. Here, I found modest evidence for sensory bias. Selection for a particular foraging preference resulted in increased mating preference for similarly colored mates. However, the correlated responses were small and inconsistent. Selection on foraging preferences alone may affect initial levels of mating preferences, but these correlations did not constrain the joint evolution of foraging and mating preferences in these simulations.     

A foraging advantage for dichromatic marmosets (Callithrix geoffroyi) at low light intensity

Most New World monkey species have both dichromatic and trichromatic individuals present in the same population. The selective forces acting to maintain the variation are hotly debated and are relevant to the evolution of the ‘routine’ trichromatic colour vision found in catarrhine primates. While trichromats have a foraging advantage for red food compared with dichromats, visual tasks which dichromats perform better have received less attention. Here we examine the effects of light intensity on foraging success among marmosets. We find that dichromats outperform trichomats when foraging in shade, but not in sun. The simplest explanation is that dichromats pay more attention to achromatic cues than trichromats. However, dichromats did not show a preference for foraging in shade compared with trichromats. Our results reveal several interesting parallels with a recent study in capuchin monkeys (Cebus capucinus), and suggest that dichromat advantage for certain tasks contributes to maintenance of the colour vision polymorphism.     

Importance of achromatic contrast in short-range fruit foraging of primates

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.