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.      

Seeing red: behavioral evidence of trichromatic color vision in strepsirrhine primates

Among primates, catarrhines (Old World monkeys and apes) andcertain platyrrhines (New World monkeys) possess trichromaticcolor vision, which might confer important evolutionary advantages,particularly during foraging. Recently, a polymorphism has beenshown to shift the spectral sensitivity of the X-linked opsinprotein in certain strepsirrhines (e.g., Malagasy lemurs); however,its behavioral significance remains unknown. We assign genotypesat the X-linked variant to 45 lemurs, representing 4 species,and test if the genetic capacity for trichromacy impacts foragingperformance, particularly under green camouflage conditionsin which red detection can be advantageous. We confirm polymorphismat the critical site in sifakas and ruffed lemurs and fail tofind this polymorphism in collared lemurs and ring-tailed lemurs.We show that this polymorphism may be linked to "behavioraltrichromacy" in heterozygous ruffed lemurs but find no comparableevidence in a single heterozygous sifaka. Despite their putativedichromatic vision, female collared lemurs were surprisinglyefficient at retrieving both red and green food items undercamouflage conditions. Thus, species-specific feeding ecologiesmay be as important as trichromacy in influencing foraging behavior.Although the lemur opsin polymorphism produced measurable behavioraleffects in at least one species, the ruffed lemur, these effectswere modest, consistent with the modest shift in spectral sensitivity.Additionally, the magnitude of these effects varied across individualsof the same genotype, emphasizing the need for combined geneticand behavioral studies of trichromatic vision. We conclude thattrichromacy may be only one of several routes toward increasedforaging efficiency in visually complex environments.     

Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory

Primates possess remarkably variable color vision, and the ecological and social factors shaping this variation remain heavily debated. Here, we test whether central tenants of the folivory hypothesis of routine trichromacy hold for the foraging ecology of howler monkeys. Howler monkeys (genus Alouatta) and paleotropical primates (Parvorder: Catarrhini) have independently acquired routine trichromacy through fixation of distinct mid‐ to long‐wavelength‐sensitive (M/LWS) opsin genes on the X‐chromosome. The presence of routine trichromacy in howlers, while other diurnal neotropical monkeys (Platyrrhini) possess polymorphic trichromacy, is poorly understood. A selective force proposed to explain the evolution of routine trichromacy in catarrhines—reliance on young, red leaves—has received scant attention in howlers, a gap we fill in this study. We recorded diet, sequenced M/LWS opsin genes in four social groups of Alouatta palliata, and conducted colorimetric analysis of leaves consumed in Sector Santa Rosa, Costa Rica. For a majority of food species, including Ficus trees, an important resource year‐round, young leaves were more chromatically conspicuous from mature leaves to trichromatic than to hypothetical dichromatic phenotypes. We found that 18% of opsin genes were MWS/LWS hybrids; when combined with previous research, the incidence of hybrid M/LWS opsins in this species is 13%. In visual models of food discrimination ability, the hybrid trichromatic phenotype performed slightly poorer than normal trichromacy, but substantially better than dichromacy. Our results provide support for the folivory hypothesis of routine trichromacy. Similar ecological pressures, that is, the search for young, reddish leaves, may have driven the independent evolution of routine trichromacy in primates on separate continents. We discuss our results in the context of balancing selection acting on New World monkey opsin genes and hypothesize that howlers experience stronger selection against dichromatic phenotypes than other sympatric species, which rely more heavily on cryptic foods.     

Evolutionary renovation of L/M opsin polymorphism confers a fruit discrimination advantage to ateline New World monkeys

New World monkeys exhibit prominent colour vision variation due to allelic polymorphism of the long‐to‐middle wavelength (L/M) opsin gene. The known spectral variation of L/M opsins in primates is broadly determined by amino acid composition at three sites: 180, 277 and 285 (the ‘three‐sites’ rule). However, two L/M opsin alleles found in the black‐handed spider monkeys (Ateles geoffroyi) are known exceptions, presumably due to novel mutations. The spectral separation of the two L/M photopigments is 1.5 times greater than expected based on the ‘three‐sites’ rule. Yet the consequence of this for the visual ecology of the species is unknown, as is the evolutionary mechanism by which spectral shift was achieved. In this study, we first examine L/M opsins of two other Atelinae species, the long‐haired spider monkeys (A. belzebuth) and the common woolly monkeys (Lagothrix lagotricha). By a series of site‐directed mutagenesis, we show that a mutation Y213D (tyrosine to aspartic acid at site 213) in the ancestral opsin of the two alleles enabled N294K, which occurred in one allele of the ateline ancestor and increased the spectral separation between the two alleles. Second, by modelling the chromaticity of dietary fruits and background leaves in a natural habitat of spider monkeys, we demonstrate that chromatic discrimination of fruit from leaves is significantly enhanced by these mutations. This evolutionary renovation of L/M opsin polymorphism in atelines illustrates a previously unappreciated dynamism of opsin genes in shaping primate colour vision.     

Demonstration of a genotype-phenotype correlation in the polymorphic color vision of a non-callitrichine New World monkey, capuchin (Cebus apella)

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.     

Color Vision Variation as Evidenced by Hybrid L/M Opsin Genes in Wild Populations of Trichromatic Alouatta New World Monkeys

Platyrrhine (New World) monkeys possess highly polymorphic color vision owing to allelic variation of the single-locus L/M opsin gene on the X chromosome. Most species consist of female trichromats and female and male dichromats. Howlers (genus Alouatta) are an exception; they are considered to be routinely trichromatic with L and M opsin genes juxtaposed on the X chromosome, as seen in catarrhine primates (Old World monkeys, apes, and humans). Yet it is not known whether trichromacy is invariable in howlers. We examined L/M opsin variation in wild howler populations in Costa Rica and Nicaragua (Alouatta palliata) and Belize (A. pigra), using fecal DNA. We surveyed exon 5 sequences (containing the diagnostic 277th and 285th residues for λ_max) for 8 and 18 X chromosomes from Alouatta palliata and A. pigra, respectively. The wavelengths of maximal absorption (λ_max) of the reconstituted L and M opsin photopigments were 564 nm and 532 nm, respectively, in both species. We found one M–L hybrid sequence with a recombinant 277/285 haplotype in Alouatta palliata and two L–M hybrid sequences in A. pigra. The λ_max values of the reconstituted hybrid photopigments were in the range of 546~554 nm, which should result in trichromat phenotypes comparable to those found in other New World monkey species. Our finding of color vision variation due to high frequencies of L/M hybrid opsin genes in howlers challenges the current view that howlers are routine and uniform trichromats. These results deepen our understanding of the evolutionary significance of color vision polymorphisms and routine trichromacy and emphasize the need for further assessment of opsin gene variation as well as behavioral differences among subtypes of trichromacy.     

Alouatta Trichromatic Color Vision: Cone Spectra and Physiological Responses Studied with Microspectrophotometry and Single Unit Retinal Electrophysiology

The howler monkeys (Alouatta sp.) are the only New World primates to exhibit routine trichromacy. Both males and females have three cone photopigments. However, in contrast to Old World monkeys, Alouatta has a locus control region upstream of each opsin gene on the X-chromosome and this might influence the retinal organization underlying its color vision. Post-mortem microspectrophotometry (MSP) was performed on the retinae of two male Alouatta to obtain rod and cone spectral sensitivities. The MSP data were consistent with only a single opsin being expressed in each cone and electrophysiological data were consistent with this primate expressing full trichromacy. To study the physiological organization of the retina underlying Alouatta trichromacy, we recorded from retinal ganglion cells of the same animals used for MSP measurements with a variety of achromatic and chromatic stimulus protocols. We found MC cells and PC cells in the Alouatta retina with similar properties to those previously found in the retina of other trichromatic primates. MC cells showed strong phasic responses to luminance changes and little response to chromatic pulses. PC cells showed strong tonic response to chromatic changes and small tonic response to luminance changes. Responses to other stimulus protocols (flicker photometry; changing the relative phase of red and green modulated lights; temporal modulation transfer functions) were also similar to those recorded in other trichromatic primates. MC cells also showed a pronounced frequency double response to chromatic modulation, and with luminance modulation response saturation accompanied by a phase advance between 10–20 Hz, characteristic of a contrast gain mechanism. This indicates a very similar retinal organization to Old-World monkeys. Cone-specific opsin expression in the presence of a locus control region for each opsin may call into question the hypothesis that this region exclusively controls opsin expression.     

Advantage of dichromats over trichromats in discrimination of color-camouflaged stimuli in nonhuman primates

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 variations in Old and New World primates

It has long been recognized that there are significant individual variations in color vision among humans. Recently, even more widespread individual variation in color vision has been found to occur in members of several genera of New World monkeys. This article addresses the question of whether a representative genus of Old World monkeys, Macaca, expresses individual variations in color vision. The principal approach was to compare behavioral measurements of increment-threshold spectral sensitivity for large samples of squirrel monkeys (Saimiri sp.) and macaque monkeys (Macaca mulatta, M. fascicularis). We conclude that, if they occur at all, individual variations in color vision among macaque monkeys must be rare.     

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.     

Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates

Olfactory receptor (OR) genes constitute the molecular basis for the sense of smell and are encoded by the largest gene family in mammalian genomes. Previous studies suggested that the proportion of pseudogenes in the OR gene family is significantly larger in humans than in other apes and significantly larger in apes than in the mouse. To investigate the process of degeneration of the olfactory repertoire in primates, we estimated the proportion of OR pseudogenes in 19 primate species by surveying randomly chosen subsets of 100 OR genes from each species. We find that apes, Old World monkeys and one New World monkey, the howler monkey, have a significantly higher proportion of OR pseudogenes than do other New World monkeys or the lemur (a prosimian). Strikingly, the howler monkey is also the only New World monkey to possess full trichromatic vision, along with Old World monkeys and apes. Our findings suggest that the deterioration of the olfactory repertoire occurred concomitant with the acquisition of full trichromatic color vision in primates.     

Genetic variability of the sws1 cone opsin gene among New World monkeys

Vision is a major sense for Primates and the ability to perceive colors has great importance for the species ecology and behavior. Visual processing begins with the activation of the visual opsins in the retina, and the spectral absorption peaks are highly variable among species. In most Primates, LWS/MWS opsins are responsible for sensitivity to long/middle wavelengths within the visible light spectrum, and SWS1 opsins provide sensitivity to short wavelengths, in the violet region of the spectrum. In this study, we aimed to investigate the genetic variation on the sws1 opsin gene of New World monkeys (NWM) and search for amino acid substitutions that might be associated with the different color vision phenotypes described for a few species. We sequenced the exon 1 of the sws1 opsin gene of seven species from the families Callitrichidae, Cebidae, and Atelidae, and searched for variation at the spectral tuning sites 46, 49, 52, 86, 90, 93, 114, 116, and 118. Among the known spectral tuning sites, only residue 114 was variable. To investigate whether other residues have a functional role in the SWS1 absorption peak, we performed computational modeling of wild-type SWS1 and mutants A50I and A50V, found naturally among the species investigated. Although in silico analysis did not show any visible effect caused by these substitutions, it is possible that interactions of residue 50 with other sites might have some effect in the spectral shifts in the order of ~14 nm, found among the NWM. We also performed phylogenetic reconstruction of the sws1 gene, which partially recovered the species phylogeny. Further studies will be important to uncover the mutations responsible for the phenotypic variability of the SWS1 of NWM, and how spectral tuning may be associated with specific ecological features such as preferred food items and habitat use.     

Evolution of activity patterns and chromatic vision in primates: morphometrics, genetics and cladistics

Hypotheses for the adaptive origin of primates have reconstructed nocturnality as the primitive activity pattern for the entire order based on functional/adaptive interpretations of the relative size and orientation of the orbits, body size and dietary reconstruction. Based on comparative data from extant taxa this reconstruction implies that basal primates were also solitary, faunivorous, and arboreal. Recently, primates have been hypothesized to be primitively diurnal, based in part on the distribution of color-sensitive photoreceptor opsin genes and active trichromatic color vision in several extant strepsirrhines, as well as anthropoid primates (Tan & Li, 1999 Nature402, 36; Li, 2000 Am. J. phys. Anthrop. Supple.30, 318). If diurnality is primitive for all primates then the functional and adaptive significance of aspects of strepsirrhine retinal morphology and other adaptations of the primate visual system such as high acuity stereopsis, have been misinterpreted for decades. This hypothesis also implies that nocturnality evolved numerous times in primates. However, the hypothesis that primates are primitively diurnal has not been analyzed in a phylogenetic context, nor have the activity patterns of several fossil primates been considered.This study investigated the evolution of activity patterns and trichromacy in primates using a new method for reconstructing activity patterns in fragmentary fossils and by reconstructing visual system character evolution at key ancestral nodes of primate higher taxa. Results support previous studies that reconstruct omomyiform primates as nocturnal. The larger body sizes of adapiform primates confound inferences regarding activity pattern evolution in this group. The hypothesis of diurnality and trichromacy as primitive for primates is not supported by the phylogenetic data. On the contrary, nocturnality and dichromatic vision are not only primitive for all primates, but also for extant strepsirrhines. Diurnality, and possibly X-linked polymorphic trichromacy, evolved at least in the stem lineage of Anthropoidea, or the stem lineage of all haplorhines.     

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.     

New World Monkeys and Color

The visual worlds of most primates are rich with potential color signals, and many representatives of the order have evolved the biological mechanisms that allow them to exploit these sources of information. Unlike the catarrhines, platyrrhines typically have sex-linked polymorphic color vision that provides individuals with any of several distinct types of color vision, including both trichromatic and dichromatic variants. In recent years, this polymorphism has been the target of an expanding range of research efforts. As a result, researchers now reasonably understand the proximate biology underlying the polymorphisms, and a number of ideas have emerged as to their evolution. Progress has also been made in illuminating how color vision capacities may be related to the particular visual tasks that New World monkeys face.     

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.     

非人灵长类动物种质冷冻保存研究进展和展望

非人灵长类动物是生物多样性的重要组成部分,也是生物医学研究的珍贵实验动物,然而,由于人类活动、栖息地破坏、狩猎和遗传隔离等原因,许多非人灵长类动物的野生种群数量急剧下降,甚至处于灭绝的边缘。种质冷冻保存对拯救非人灵长类动物和保存遗传物质资源具有重要意义。本文综述了新大陆猴、旧大陆猴和巨猿等类群动物精子、卵子、胚胎和性腺组织等种质冷冻保存的研究进展,介绍了狨猴、松鼠猴、恒河猴、食蟹猴和黑猩猩等种质冷冻保存的主要方法,并对未来种质冷冻保存的研究方向进行了讨论。     

Divergent selection for opsin gene variation in guppy (Poecilia reticulata) populations of Trinidad and Tobago

The guppy is known to exhibit remarkable interindividual variations in spectral sensitivity of middle to long wavelength-sensitive (M/LWS) cone photoreceptor cells. The guppy has four M/LWS-type opsin genes (LWS-1, LWS-2, LWS-3 and LWS-4) that are considered to be responsible for this sensory variation. However, the allelic variation of the opsin genes, particularly in terms of their absorption spectrum, has not been explored in wild populations. Thus, we examined nucleotide variations in the four M/LWS opsin genes as well as blue-sensitive SWS2-B and ultraviolet-sensitive SWS1 opsin genes for comparison and seven non-opsin nuclear loci as reference genes in 10 guppy populations from various light environments in Trinidad and Tobago. For the first time, we discovered a potential spectral variation (180 Ser/Ala) in LWS-1 that differed at an amino acid site known to affect the absorption spectra of opsins. Based on a coalescent simulation of the nucleotide variation of the reference genes, we showed that the interpopulation genetic differentiation of two opsin genes was significantly larger than the neutral expectation. Furthermore, this genetic differentiation was significantly related to differences in dissolved oxygen (DO) level, and it was not explained by the spatial distance between populations. The DO levels are correlated with eutrophication that possibly affects the color of aquatic environments. These results suggest that the population diversity of opsin genes is significantly driven by natural selection and that the guppy could adapt to various light environments through color vision changes.     

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.     

Visual pigment evolution in Characiformes: The dynamic interplay of teleost whole‐genome duplication,surviving opsins and spectral tuning

Vision represents an excellent model for studying adaptation, given the genotype‐to‐phenotype map that has been characterized in a number of taxa. Fish possess a diverse range of visual sensitivities and adaptations to underwater light, making them an excellent group to study visual system evolution. In particular, some speciose but understudied lineages can provide a unique opportunity to better understand aspects of visual system evolution such as opsin gene duplication and neofunctionalization. In this study, we showcase the visual system evolution of neotropical Characiformes and the spectral tuning mechanisms they exhibit to modulate their visual sensitivities. Such mechanisms include gene duplications and losses, gene conversion, opsin amino acid sequence and expression variation, and A₁/A₂‐chromophore shifts. The Characiforms we studied utilize three cone opsin classes (SWS2, RH2, LWS) and a rod opsin (RH1). However, the characiform's entire opsin gene repertoire is a product of dynamic evolution by opsin gene loss (SWS1, RH2) and duplication (LWS, RH1). The LWS‐ and RH1‐duplicates originated from a teleost specific whole‐genome duplication as well as characiform‐specific duplication events. Both LWS‐opsins exhibit gene conversion and, through substitutions in key tuning sites, one of the LWS‐paralogues has acquired spectral sensitivity to green light. These sequence changes suggest reversion and parallel evolution of key tuning sites. Furthermore, characiforms' colour vision is based on the expression of both LWS‐paralogues and SWS2. Finally, we found interspecific and intraspecific variation in A₁/A₂‐chromophores proportions, correlating with the light environment. These multiple mechanisms may be a result of the diverse visual environments where Characiformes have evolved.