Genetics and Evolution of Color Vision in Primates
Summary and Keywords
Color is a central feature of human perceptual experience where it functions as a critical component in the detection, identification, evaluation, placement, and appreciation of objects in the visual world. Its role is significantly enhanced by the fact that humans evolved a dimension of color vision beyond that available to most other mammals. Many fellow primates followed a similar path and in recent years the basic mechanisms that support color vision—the opsin genes, photopigments, cone signals, and central processing—have been the subjects of hundreds of investigations. Because of the tight linkage between opsin gene structure and the spectral sensitivity of cone photopigments, it is possible to trace pathways along which color vision may have evolved in primates. In turn, such information allows the development of hypotheses about the nature of color vision and its utility in nonhuman primates. These hypotheses are being critically evaluated in field studies where primates solve visual problems in the presence of the full panoply of photic cues. The intent of this research is to determine which aspects of these cues are critically linked to color vision and how their presence facilitates, impedes, or fails to influence the solutions. These investigations are challenging undertakings and the emerging literature is replete with contradictory conclusions. But steady progress is being made and it appears that (a) some of the original ideas about there being a restricted number of tasks for which color vision might be optimally utilized by nonhuman primates (e. g., fruit harvest) were too simplistic and (b) depending on circumstances that can include both features of proximate visual stimuli (spectral cues, luminance cues, size cues, motion cues, overall light levels) and situational variables (social cues, developmental status, species-specific traits) the utilization of color vision by nonhuman primates is apt to be complex and varied.
Laboratory investigations of human color vision started in the late 17th century. In the years that followed, that topic became one of the most thoroughly studied aspects of human perceptual experience. Despite the long-term interest in human color vision, it was not until the early 20th century that studies of color vision in nonhuman primates were initiated, principally by Kinnaman (1902) and Watson (1909), each of whom conduced discrimination tests on captive macaque monkeys. Both found their subjects could make true color discriminations. Trendelenberg and Schmidt (1930) and Grether (1939) later conducted investigations that established that the color vision of Old World monkeys is like that of humans who have normal color vision. There was sporadic interest in the color vision of nonhuman primates in the years following these two pioneering investigations, but it was the advent and application of an array of new experimental techniques—both biologically and behaviorally based—in the late 20th century that led to an understanding of the scope and nature of primate color vision. Those later advances are considered here.
Like all phylogenies, those for the Order Primates undergo continuous revision as new techniques and richer databases emerge. Recent estimates place the origin of primates in the Late Cretaceous, around 74 million years ago, with a subsequent rapid radiation following the Cretaceous/Paleogene (K/Pg) extinction event of 66 million years ago. Some 400 primate species are currently recognized. Reflecting the body of research on color vision, the discussion here deals with a small number of strepsirrhines and haplorrhines. The former includes the lorises, lemurs, and bushbabies; the latter, tarsiers, platyrrhines (New World monkeys), and catarrhines (apes, Old World monkeys, humans).
Color Vision Formalities
A framework for understanding color vision was established by Newton’s early results on color mixing, which showed that human color vision has a dimensional character, and by Thomas Young’s subsequent suggestion that Newton’s suggestion might be explained by the presence of three independent biological analyzers. Through demonstrations that variations in the proportions of only three fixed spectral primaries are required to match the appearance of all other spectral lights, Helmholtz and Maxwell later showed that human color vision is indeed trichromatic. During the early part of the 20th century opinion converged on the idea that the initial stage in the visual system underlying trichromacy was the presence of three classes of cone, each containing a spectrally unique photopigment. In the early 1960s, these three were conclusively identified by the direct measurements of the absorption properties of single cones (Brown & Wald, 1964; Marks, Dobelle, & MacNichol, 1964). Inherited variations in human color vision, characterized by alterations in dimensionality from the trichromatic norm (dichromatic, monochromatic), or by changes in the proportions of mixture primaries required to complete color matches (variant forms of trichromacy and dichromacy), could also be explained by alterations in the number of cone pigment types or by shifts in photopigment spectral positioning.
In early color-vision experiments conducted on a few other common species (e. g., bees, pigeons, goldfish), this relationship between the number and spectral properties of photopigments was found to be similarly linked to the dimensionality and nature of their color vision (Kelber & Jacobs, 2016). As technological advances allowed rapid assessments of the number and spectral properties of photopigments in various species, this linkage has been frequently relied on to predict or assert the nature of color vision. At the same time, however, abundant evidence has emerged that shows such assumptions can be badly misled and frequently fail to appreciate the scope and complexity of color vision and its biological concomitants across the animal kingdom (Jacobs, 2018; Marshall & Arikawa, 2014; Menzel & Backhaus, 1991).
Beyond color matching, a technique fundamental to establishing dimensionality, many other derived aspects of color vision have been studied over the years. These include discrimination measures that index the acuteness of color vision and, particularly in the case of human subjects, a broad array of behaviors that require cognitive judgments of color (Elliott, Fairchild, & Franklin, 2015; Webster, 2018).
Overview of Vertebrate Opsin-Gene Evolution
Photopigment molecules are G-protein-coupled receptors consisting of a protein, opsin, covalently bound to a chromophore. Results from early studies of color vision defects in humans showed that variations in photopigments have a heritable component. It was subsequently hypothesized that variations in photopigment structure are responsible for shifts in the spectral tuning of photopigments (Neitz & Neitz, 2011). Starting in the mid-1980s, advances in molecular biology allowed a determination of how opsin gene structure links to photopigment function. Since that time, opsin genes obtained from many animals have been isolated and sequenced (e. g., Porter et al., 2012). Comparisons of these sequences in turn fostered the development of opsin-gene phylogenies that can be used to illuminate the evolution of opsins and, by extension, allow insight into the probable course of the evolution of color vision.
The emergence of opsins has been dated to around 800 million years ago (Feuda, Hamilton, McInerney, & Pisani, 2012). The ancestral vertebrate visual opsin gene is argued to have duplicated at a time close to the appearance of the vertebrates (~525 million years ago). Four families of cone-opsin genes subsequently emerged as a result of various gene gains and losses and two rounds of whole genome duplications (Lamb, 2013). Opsin-gene representatives from these four specify all contemporary vertebrate cone pigments. By convention, these are identified as SWS1, SWS2, Rh2, and LWS. As a group, these genes provide cone pigments whose spectral peak absorptions (λmax) lie in the range of about 355-560 nanometers (nm) (Figure 1.) An additional gene family, Rh1, evolved from SWS1 opsin genes. Rh1 genes specify rod photopigments, which have spectral peaks of about 500 nm.
Although representative genes drawn from all four of the cone opsin families have been retained in some vertebrate lineages (e. g., various fishes, birds, and reptiles), the evolution of mammalian cone opsin genes has been principally characterized by loss of representation (Figure 2). Rh2 genes disappeared from primitive mammals at a (so far) unspecified time point, leaving crown mammals with representation from only three opsin gene families. SWS2 opsin genes were subsequently lost from metatherians (marsupials and placentals), while SWS1 disappeared from the prototherian (monotreme) lineage. A consequence of these losses is that representatives from only two cone opsin gene families survive in modern mammals (Jacobs, 2009).
Evolution and Spectral Tuning of Primate Photopigments
Pioneering investigations by Nathans and colleagues isolated and sequenced cone-opsin genes from both color-normal and color-defective humans (Nathans, Piantanida, et al., 1986; Nathans, Thomas, & Hogness, 1986). As predicted from earlier studies of color vision defects, two genes drawn from the LWS gene family were localized to the X chromosome (Xq28). These genes underlie the L and M cone pigments (respective λmax of ~560 and 530 nm). The L- and M-opsin genes (OPN1LW and OPN1MW) have a 98% nucleotide sequence identity and are aligned in tandem with OPN1LW in the upstream position. Through a comparison of the sequences of the L- and M-opsin genes in several color-normal males, Nathans, Piantanida, et al. (1986) found that whereas the L-opsin gene is present as a single copy, some individuals may have one or more copies of the M-opsin genes.
Smallwood, Wang, and Nathans (2002) and Wang et al. (1992) unveiled the mechanisms supporting differential expression of OPN1LW and OPN1MW. Each of these genes contains a flanking promotor region that directs expression. An upstream locus control region (LCR) pairs stochastically with each of these promotors to determine which of the two genes is expressed in any given cone.
The L- and M-opsin genes each contain six exons and encode proteins consisting of a polypeptide chain of 364 amino acids. Variations in the spectral tuning of the M and L pigments in primates are largely due to a small number of amino acid substitutions. The major share of the approximately 30 nm spectral difference between M and L pigments arises from sequence variations in exons 3 and 5 of the M and L opsins that result in amino acid substitutions between polar and nonpolar residues at positions 180 (Ser/Ala), 277 (Tyr/Phe), and 285 (Thr/Ala) (Neitz, Neitz, & Jacobs, 1991). The polar residues mostly characterize the L pigments, the nonpolar residues the M pigments. Each of these changes results in a discrete shift in spectral tuning of the pigment. For example, substituting Ala for Ser in the L pigment leads to a shift of the photopigment peak of approximately 3 to 4 nm toward shorter wavelengths (Merbs & Nathans, 1992; Neitz et al., 1991; Sanocki et al., 1993). The total shift in the pigment peaks of the M and L pigments is roughly the algebraic sum of the shifts engendered by substitutions at each of these three sites (Asenjo, Rim, & Oprian, 1994; Neitz et al., 1991). In addition, a handful of other substitutions and their combinations can result in small shifts in the spectral peaks of the human M and L pigments (Davidoff, Neitz, & Neitz, 2016; Neitz & Neitz, 2011).
The gene from the SWS1 family that forms the S-cone opsin maps to an autosome (at 7q32) and codes for the third cone pigment. The S-cone opsin gene (OPN1SW) has a nucleotide sequence identity of about 40% with OPN1MW and OPN1LW, has five exons, and encodes an opsin of 348 amino acids (Nathans, Thomas, et al., 1986). The consensus is that the ancestral SWS1 opsin gene formed the basis for photopigments that peak in the ultraviolet (UV). Some mammals retain UV-sensitive pigments (with λmax of ~360 nm); but in others, including all primates, substitutions in the SWS1 opsin sequences have resulted in a photopigment shift into the visible wavelengths (Hunt, Carvallo, Cowing, & Davies, 2009). The exact substitutions—or combinations—underlying these spectral shifts in the primate SWS1 pigments remain under study (Carvahlo, Davies, Robinson, & Hunt, 2012).
The spectral positioning of primate S cone pigments varies across species with peak values covering the range from about 410 nm to 435 nm. The shortest of the primate S-cone pigments thus far measured is from the aye-aye (Daubentonia medagascariensis), a nocturnal strepsirrhine with an S-cone pigment peaking at 406 nm (Carvahlo et al., 2012). Of the two catarrhines most often studied in color vision research, the human S-cone pigment peaks in the region of 414 to 419 nm as measured with microspectrophotometry (MSP) or in vitro pigment regeneration (Dartnall, Bowmaker, & Mollon, 1983; Fasick, Lee, & Oprian, 1999), while measurements of the absorption properties of S-cone recombinant photopigment expressed in tissue culture gave a peak estimate of 426 nm (Merbs & Nathans, 1992). MSP and suction electrode recordings from the S-cones of macaque monkeys (Macaca sp.) gave peaks at about 430 nm (Baylor, Nunn, & Schnapf, 1984; Bowmaker, Astell, Hurst, & Mollon, 1991). There are few direct measurements of S-cone photopigments in platyrrhine monkeys. MSP recordings yielded average spectral peaks of 436 nm and 423 nm for squirrel monkeys (Saimiri sciureus) and marmosets (Callithrix jacchus), respectively (Mollon, Bowmaker, & Jacobs, 1984; Tovee, Bowmaker, & Mollon, 1992).
Spectral Peak Measurements
Because the spectral sensitivity curves of photopigments transform to a common shape, they are typically specified by the wavelength of their spectral peak (λmax). As illustrated in the examples cited earlier, estimates obtained for what are ostensibly the same photopigments often vary. Part of that variability reflects inherent measurement error. Beyond that, peak estimates have been obtained using a variety of techniques, from in vitro measurements of recombinant pigments made with a spectrophotometer to in vivo measurements obtained from intact eyes using various electrophysiological or psychophysical approaches. Although these estimates are sometimes treated as directly comparable, each has limitations and utilities.
Whereas the in vitro techniques may seem the most precise, they fail to capture the spectral filtering effects on light as it passes through an intact eye prior to photopigment activation. The influence of these filters can be important in drawing inferences about vision, including color vision. Most relevant is the fact that the lenses in primate eyes, at least those for all the diurnal species, introduce pronounced differential attenuation of short-wavelength lights (Cooper & Robson, 1969; Douglas & Jeffrey, 2014). The lens of the macaque monkey, for instance, falls to 50% of its maximum long-wavelength transmission at 424 nm, then drops very steeply below that figure across progressively shorter wavelengths. Additionally, most primate eyes contain a prominent intraretinal filter, the macular pigment, which is centered on the fovea and extends over a total area of some 7 to 8 degrees. Macular pigment absorbs maximally at 460 nm where its transmittance drops to about 35% to 40% of its maximum (Snodderly, Brown, Delori, & Auran, 1984).
Van de Kraats and van Norren (2007) compiled data that summarizes the absorbance of light by all the ocular media in the human eye. As illustrated in Figure 3, absorbance in the media rises steeply in the short wavelengths. The result of this filtering is that the maximum sensitivity of the human S-cone is long-wavelength shifted some 20 nm from the value of around 420 nm derived from direct pigment measurements to a peak value of about 442 nm obtained from color matching (Stockman & Brainard, 2010). Similar effects can be expected to impact fundamental characteristics of color vision in other primates and they require consideration in attempts to link photopigment absorption to seeing.
Temporal Niche of Early Primates
Characteristic features of eyes and visual systems reflect the demands and opportunities provided by photic environments over time. Consequently, there has been considerable interest in understanding the photic worlds of early primates. Gordon Walls (1942) first noted that the eyes and visual systems of mammals differed from those of other terrestrial vertebrates in ways that implied that all mammals shared a nocturnal ancestry. According to most accounts, mammals first appeared about 250 million years ago and the period of their nocturnality extended from sometime after that point throughout the Mesozoic until the K/Pg extinction event of 66 million years ago (Gerkema, Davies, Foster, Menaker, & Hut, 2013). Perhaps keyed by competition from diurnal reptiles (Schwab, 2012), that period is typically characterized as constituting a “nocturnal bottleneck” for mammals. In accord with this nocturnality, the changes induced in mammalian biology included the evolution of endothermia, alterations in eye configuration, retinal photoreceptor composition, the expansion of tactile and olfactory capacities, the reorganization of photic inputs to circadian control mechanisms, and a reduction in cone-opsin gene representation (Anderson & Wiens, 2017; Bickelmann et al., 2015; Hall, Kamilar, & Kirk, 2012; Maor, Dayan, Ferguson-Gow, & Jones, 2017).
Many contemporary primates are diurnal (all catarrhines, most platyrrhines, a few strepsirrhines), others are nocturnal (tarsier, a single platyrrhine genus, numerous strepsirrhines), and a smaller number (e.g., the strepsirrhines, lemur and eulemur) are usually judged to be cathemeral. The last common ancestor of all primates was classically assumed to have been nocturnal, with shifts to other states evolving secondarily (e.g., Crompton, 1995). That conclusion is buttressed by results from studies of eye and orbit shape and through analysis of the activity patterns of contemporary primates (Heesy & Hall, 2010; Santini, Rojas, & Donzati, 2015). Alternatively, claims derived from studies of opsin-gene patterns suggest the earliest primates may have been either diurnal or cathemeral (Tan, Yoder, Yamashita, & Li, 2005; Melin, Matsushita, Moritz, Dominy, & Kawamura, 2013). Whether the earliest primates were nocturnal, cathemeral, diurnal, or some admixture of the three, various lineages have over the years evolved the capacities to survive and prosper in a broad range of photic habitats.
Nathans, Thomas, et al. (1986) pointed out that the sequence identities and juxtaposition of the human M and L opsin genes on the X chromosome implied they emerged from a recent gene duplication. Prior to their work, it had been established that the cone-opsin gene complements of representative platyrrhine monkeys differ fundamentally from those characteristic of catarrhines (Jacobs & Neitz, 1985; Mollon et al., 1984), so the hypothesized duplication event must have occurred after the divergence of the two lineages. The exact timing of the catarrhine/platyrrhine divergence has been much debated. Studies based on an analysis of mitochondrial genomes place that divergence at about 35 million years ago (Schrago & Russo, 2003). Crown catarrhines are estimated to have appeared 32 million years ago (Pozzi et al., 2014), suggesting that the duplication of the catarrhine X-chromosome opsin genes dates to somewhere around 30 to 35 million years ago.
Subsequent research revealed that all catarrhine M and L opsin genes and photopigments share similar features. For one thing, measurements of M and L cone spectra made across numerous species of catarrhine monkeys show they have similar spectral properties (Baylor et al., 1984; Bowmaker et al., 1991; Jacobs & Deegan, 1999). Additionally, opsin gene structures for several species of catarrhine monkeys have high homology to those of humans, and the specific sites associated with spectral tuning of the M and L pigments are the same (Dulai, Bowmaker, Mollon, & Hunt, 1994; Onishi et al., 2002). Both patterns are repeated among the apes (Deeb, Jorgensen, Battisti, Iwasaki, & Motulsky, 1994; Deegan & Jacobs, 2001; Dulai, Bowmaker, Mollon, & Hunt, 1994; Hiwatashi et al., 2011; Jacobs, Deegan, & Moran, 1996; Terao et al., 2005). It appears that the genes specifying the M and L pigments of catarrhine primates emerged early during their evolution and have in the main been selectively maintained over the years since.
Features Apparently Unique to Humans
Among the most heavily investigated features of human color vision are its deficiencies. These variant conditions are common, in some populations affecting as many as 6% to 8% of all males. Color vision defects are inherited as X-chromosome traits expressed through alterations in the number of cone types and in their spectral properties. Accordingly, the unveiling of opsin-gene structures meant that color vision defects could be directly tied to their genetic bases. In their investigation, Nathans, Piantanida, et al. (1986) pointed out that unequal intergenic or intragenic homologous recombinations occurring during meiosis could account for the gene rearrangements underlying photopigment variations linked to human color defects (Figure 4.)
Because all catarrhines share their basic opsin-gene and cone-photopigment arrangements, it is surprising that the color vision variations so common in humans are quite uncommon in other catarrhines (Jacobs & Williams, 2001; Onishi, et al., 1999; Saito, Hasegawa, Koida, Terao, & Koike, 2003). There is no agreed explanation for the difference in rates of defective color vision in human and nonhuman catarrhines. Relaxation of selection against color vision defects in modern humans that has not occurred in other catarrhines is one possibility (Neitz & Neitz, 2011; Post, 1962).
For many years, estimates of the relative prevalence of L and M cones in the human retina were obtained by fitting summative combinations of L and M cone spectra to photopic spectral sensitivity functions. These suggested L cones typically outnumber M cones. Recent investigations employing better measurement techniques validate that claim. For instance, using both genetic and electrophysiological indices, Carroll, Neitz, and Neitz (2002) found that on average there are nearly three times as many L cones as M cones in the human retina. The L:M cone ratio also varies significantly across the extent of the retina and, very strikingly, among individuals. The explanation for the disparity in the number of L and M cones remains elusive. The closer proximity of the LCR to the L-opsin gene promotor than to that for the M-opsin gene promotor was suggested as a possible mechanism for the higher frequency of L cones (Smallwood et al., 2002). However, males of African descent have opsin gene arrays like those for Caucasians but have significantly lower L:M cone ratios, so proximity cannot be the complete explanation for the mismatch in L and M cone representation (McMahon, Carroll, Awua, Neitz, & Neitz, 2008). Another possibility is that there are structural differences at some other locations in the X-chromosome opsin gene array that influence the L:M cone ratio (Gunther, Neitz, & Neitz, 2008).
Presuming that the same gene duplication established the pattern used to support the presence of M and L cones in all catarrhines, it is puzzling that the striking disparities in the relative numbers of M and L cones seen in (at least some) human populations is apparently not universal across catarrhines. For example, estimates obtained from electrophysiological measurements of macaque monkeys suggest their L:M ratios are close to 1 (Jacobs & Deegan, 1997; Lindbloom-Brown, Tait, & Horwitz, 2014). A similar L:M cone ratio was also detected in a study of chimpanzees (Jacobs, Deegan, & Moran, 1996). On the other hand, an early experiment based on a small sample of baboon retinas concluded that in this catarrhine the L:M ratio is reversed, with relatively more M than L cones (Marc & Sperling, 1977). These studies suffer from restricted sample sizes and the range of assumptions inherent in the techniques used to estimate cone numerosity. Despite that, it looks as if whatever controls L:M cone ratios varies significantly across the catarrhines.
Classically it was assumed that the X chromosome had only two genes specifying the M and L cone pigments, but the earliest molecular genetic studies showed that the total array often consists of multiple genes. Many subsequent studies have validated this view (Neitz & Neitz, 2011). Indeed, individuals who would be conventionally diagnosed as dichromatic sometimes have more than a single X-chromosome opsin gene (Neitz et al., 2004). These large arrays of L/M opsin genes are apparently the result of repeated unequal recombinations over the years, which resulted in considerable variability in the structure of these genes. Usually only the first two genes in the array are expressed (Hayashi, Motulsky, & Deeb, 1999), so this sequence reshuffling can produce a variety of L and M photopigments with differing spectral properties (Davidoff et al., 2016). Such variations can alter color vision by greater or lesser amounts.
One much-studied polymorphism involves alternate versions of genes that differ in whether Ser or Ala is present at position 180 (above), the former shifting the expressed pigment slightly longer, the latter slightly shorter. This polymorphism is common, with about half of all Caucasian males expressing either one or the other (Deeb, 2005; Sanocki, Shevell, & Winderickx, 1994). The influence of that polymorphism is enough that it can be directly detected in precise color vision tests (Neitz & Jacobs, 1986; 1990; Winderickx et al., 1992).
Whether successive rounds of unequal recombination events have produced similar variations in the L/M opsin genes of other catarrhines is uncertain. In an early experiment involving a small number of subjects, Ibbotson, Hunt, Bowmaker, and Mollon (1992) detected the presence of such variation. Yet a more recent study involving analysis of the X-chromosome opsin gene arrays of nearly 140 macaque monkeys found only six individuals in which the number of opsin genes exceeded two (Onishi et al., 2002) while an examination of gibbon L/M opsin genes found evidence for multiple copies of M opsin genes in some species, but not in others (Hiwatashi et al., 2011). It seems likely that the M/L opsin gene arrays of human and nonhuman catarrhines show significant differences—the nonhuman gene arrays remain closer to what was likely the state following the original catarrhine gene duplication, whereas those for the human acquired multiple structural changes that can alter the nature of an individual’s color vision by greater or lesser amounts.
The norm for color vision in platyrrhine monkeys is polymorphic variation. Building on Grether’s (1939) early discovery of species variations in platyrrhine color vision, later behavioral studies of squirrel monkeys and two types of Callitrichids showed that each species included both trichromatic and dichromatic individuals (Jacobs, 1984; Jacobs, Neitz, & Crognale, 1987; Tovee et al., 1992). Correlative measurements of the cone photopigments and an examination of the pattern of their inheritance revealed the proximate basis for the polymorphism (Jacobs & Neitz, 1985, 1987; Mollon et al., 1984). All animals of each species share the same S-cone photopigments, but they also have three distinct classes of M/L photopigment. Individual monkeys have any single type of pigment or any pair of them. The former has dichromatic color vision, the latter are trichromats. These phenotypes are sex-linked: all males are dichromats and females are either dichromatic or trichromatic. Inheritance patterns reveal that these platyrrhines have a single X-chromosome opsin gene site with three allelic versions of this gene. Heterozygous females then achieve trichromacy through the agency of random X-chromosome inactivation.
Measurements made on monkeys from other platyrrhine genera demonstrated the widespread presence of a similar polymorphic pattern. The sets of M/L photopigments underlying the polymorphism seem to fall into two major groupings (e.g., Figure 5.) All these platyrrhine monkeys share an M/L pigment with a peak of approximately 560 nm. In one group, including representatives from three families (Cebidae, Atelidae, Pitheciidae), the other two M/L pigments have peaks of about 550 nm and 535 nm. The other group includes various species from the family Callitrichinae, whose additional M/L pigments peak at approximately 555 nm and 543 nm. The estimated peaks for these pigments have been derived from various direct measurements, from photopigment expressions studies, and by inference from genetic data. As in the cases noted previously, these numbers vary somewhat from estimate to estimate. Compilations of these values for numerous platyrrhines are available (Carvalho, Pessoa, Mountford, Davies, & Hunt, 2017; Jacobs, 2007; Kawamura & Melin, 2017).
To study the basis for these M/L photopigment variations, comparisons were made between the deduced amino acid sequences of eight primate photopigments—those for a human deuteranope and a protanope and for the three polymorphic pigments found in squirrel monkeys and in tamarins (Neitz et al., 1991). In total, these pigments represented five spectral positions that have spectral peak values falling in a range of about 530 to 560 nm. A spectral tuning pattern emerged that followed the scheme outlined earlier, in that various substituted combinations of polar and nonpolar amino acids at just three positions (180, 277, 285) in the opsin molecule accounted for pigments tuned to each of the spectral positions derived from direct measurements. Later it became evident that additive combinations of shifts predicted from changes at these three sites account reasonably well for the measured and predicted peaks of the M/L pigments for quite a number of platyrrhine species (Jacobs, 2007), although some modest deviations from these peak values have been reported (Kawamura & Melin, 2017).
Three variations on this theme have been detected. The first involves the nocturnal Aotus monkey. Unique among the platyrrhines, Aotus has only a single cone pigment in its retina, an M/L photopigment with λmax estimated to be 539 to 543 nm (Hiramatsu, Radlwimmer, Yokoyama, & Kawamura, 2004; Jacobs, Deegan, Neitz, Crognale, & Neitz, 1993). The Aotus genome additionally contains an S-pigment opsin gene, but that gene harbors inactivating mutations that obviate its expression (Levenson, Fernandez-Duque, Evans, & Jacobs, 2007). With only a single cone photopigment, Aotus lacks color vision.
A second variation involves the number of L/M alleles. Three such alleles have been found in most platyrrhines, but there appear to be a few exceptions. Although also polymorphic, examinations of spider monkeys (Ateles sp.) that involved more than 50 animals found only two alleles (Jacobs & Deegan, 2001; Hiramatsu et al., 2005). Five different M/L photopigments were detected in an electrophysiological survey of 82 Callicebus molloch monkeys from the family Pitheciidae (Jacobs & Deegan, 2005), while a total of six opsin-gene alleles were found in a genetic survey of 52 X chromosomes surveyed from another species of this same family, the bald uakari (Cacajao calvus; Corso, Bowler, Heymann, Roos, & Mundy, 2016).
For platyrrhines, the maximum incidence of female heterozygosity is limited by the number of alleles at that site and their relative frequencies in the population. An increase in the number of alleles can in theory increase the incidence of trichromats. Further, the identity of the photopigment pairings that emerge alters the nature of the resultant color vision.
The incidence of female trichromacy is maximized if the allelic genes are equally frequent in the population. Deviations from equal frequency could reflect the evolutionary history of these genes or result from the action of selective forces favoring some genes or combinations of genes. A few studies have provided estimates of allele frequencies in various platyrrhines. Interpretation of such results requires caution as the outcomes can be biased by small sample sizes. Some assays find unequal representation for the various alleles (see Kawamura & Melin, 2017). In one case, relatively large and heterogeneous samples of allele frequencies were compiled for squirrel monkeys (Saimiri) and for several species of Callitrichids (Rowe & Jacobs, 2004). Both groups have three M/L opsin gene alleles, but they specify different arrays of M/L photopigments. The spectra of the three L/M photopigments for the squirrel monkey are reasonably equally spaced between 535 nm and 562 nm, while those of the Callitrichids M/L photopigments are not, the two longest pigments are close to one another having a peak separation of about 6 nm (Fig. 5). The 362 alleles identified for squirrel monkeys did not differ from the prediction of equal frequencies for the three alleles, but the sample of Callitrichids (n = 406) did, the middle pigment in the Callitrichid M/L pigment array (λmax = ~556 nm) being significantly underrepresented. On theoretical grounds, the lower frequency of that opsin gene is predicted to cause only relatively small changes in the overall representation of dichromats or trichromats in the population, but it significantly alters the potential gene combinations in heterozygous females with a marked increase in the pairings of the shortest and longest pigments (Rowe & Jacobs, 2004). Such a result is open to interpretation, but generally speaking putative color signals in platyrrhine visual systems become more robust as a function of the spectral separation of the photopigments involved (Blessing, Solomon, Hashemi-Nezhad, Morris, & Martin, 2004), paralleling what is found in tests of human color discrimination.
In the face of widespread polymorphic variations in platyrrhine monkeys, the third variant feature was the most unexpected. Electrophysiological and genetic tests on howler monkeys (Alouatta sp.) revealed that each animal has two X-chromosome opsin genes specifying photopigments with λmax of 530 nm and 562 nm, and predicted that howler monkeys should be “routinely trichromatic” (Jacobs, Neitz, Deegan, & Neitz, 1996). Direct measurements of cone absorption spectra and behavioral tests support this finding (Araujo et al., 2008; Silveira et al., 2014). A more recent genetic study detected a hybrid M/L opsin gene in small minority (~10%) of howler monkey X chromosomes. This suggests that occasionally a pigment peaking somewhere in the range of 546 to 554 nm may be paired with one of the two more common photopigments. Pigment pairings in other platyrrhines having much smaller spectral separations do support clear trichromatic color vision (e.g., Jacobs et al., 1987). Thus, although indeed “routinely trichromatic,” the details of howler monkey color vision may include some individual trichromatic variants.
Catarrhine primates and howler monkeys both added second opsin genes to the X-chromosome array. A comparison of the opsin gene nucleotide variants among howler monkeys, Old World monkeys, and other New World monkeys suggested that howler monkeys achieved their trichromacy independent of the events that led to catarrhine trichromacy (Jacobs et al., 1996). An independent origin of howler monkey trichromacy is also supported by the fact that, unlike the catarrhines, where a single upstream LCR pairs with L and M opsin promotors to direct expression, in the howler monkey both L and M gene have neighboring LCRs. This arrangement supports the view that howler monkey trichromacy emerged from a single-site polymorphic past (Dulai, von Dornum, Mollon, & Hunt, 1999).
After years of debate, Tarsiers are now recognized as members of the semiorder Haplorini. They have evolved independently for more than 60 million years. Tarsiers provide an attractive puzzle for vision scientists. In accordance with their nocturnality, they have large eyes that enhance light gathering, retinas that are heavily rod-dominated, and maximum cone and ganglion cell densities like those found in other nocturnal primates (Hendrickson, Djajadi, Nakamura, Possin, & Sajuthi, 2000; Tetreault, Hakeem, & Allman, 2004). But their visual systems also contain features associated with diurnality: frontally oriented orbits, an avascular fovea, no tapetum, and a relatively large primary visual cortex (Collins, Hendrickson, & Kaas, 2005). The interpretation typically offered for these seemingly contradictory arrangements is that tarsiers were at some point diurnal or crepuscular and subsequently became nocturnal.
Tan and Li (1999) discovered the presence of LWS opsin genes in tarsiers and found that the structures of the genes isolated from two genera of Tarsiers predicted two spectrally discrete M/L pigments. Further study revealed the presence of an SWS1 opsin gene and its cone pigment product was detected by antibody labeling (Tan et al., 2005). These findings have been replicated and a twofold interpretation offered: (1) contemporary tarsiers have dichromatic color vision, and (2) the presence of different LWS photopigments in different genera implies that an ancestral species must have had polymorphic color vision characterized by the presence of both trichromatic and dichromatic females in a fashion similar to that detected in platyrrhine monkeys (Melin et al., 2013; Moritz, Ong, Perry, & Dominy, 2017).
The inferences drawn about tarsier color vision are buttressed by appeals to natural history, by analogies to the platyrrhines, and by modeling of the tarsier visual environment. The speculation about a trichromatic past for Tarsius cannot be directly evaluated and the presumed dichromacy of modern tarsiers has not yet been established. Here, as in other cases, the presence of two classes of cones (S and M/L) is often taken as prima facie evidence for dichromatic color vision. The tarsier retinal structure suggests grounds for caution in reaching that conclusion. Beyond their overall sparsity, the distributions of two tarsier cone types are highly atypical (Hendrickson et al., 2000). Note in Figure 6 that the spatial distributions for S and M/L cones are nearly reciprocal, the highest concentrations of M/L cones being around the fovea with, remarkably, S cones virtually absent across the entire central portion of the retina. It is not known how tarsier cones are wired into retinal circuitry, but the photoreceptor distribution of Figure 6 would seem to offer somewhat limited prospects for neural comparisons of signals from two cone types sampling the common locations in visual space, an arrangement ordinarily required to generate robust color signals. Tarsiers may well achieve some degree of dichromatic color vision, but the anatomical picture suggests that this should be a hypothesis and is not a given.
Primates of the suborder Strepsirrhini diverged from the haplorrhines early in primate history. Their eyes generally lack foveas, contain reflective tapeta, and have relatively low cone:rod ratios. There is wide variation across species in the density and retinal distribution of cones that correlates with the photic rhythmicity of the species; however, even in the most diurnal species, cone density does not achieve the levels found in the anthropoids (Peichl et al., 2019).
In recent years strepsirrhine opsin genes have come under study. Mutational changes in the SWS opsin genes of galagos, lorises, and dwarf lemurs—all strongly nocturnal species—render them nonfunctional (Jacobs, Neitz, & Neitz, 1996; Kawamura & Kubotera, 2004; Tan et al., 2005). As far as is now known, all other strepsirrhines have functional S cones and some M/L cone representation. Tan and Li (1999) examined the LWS genes in 20 strepsirrhines and discovered that although many of the species have only a single LWS opsin gene, two of the lemuriforms they examined had allelic versions of the LWS opsin gene, implying that heterozygous females might achieve trichromatic color vision in a fashion similar to that of platyrrhine monkeys. The polymorphism so detected involved amino-acid substitutions at a single location (site 285, Thr/Ala). That finding was validated and extended in several subsequent studies (Kawamura & Melin, 2017). A recent study examined LWS opsin genes from nine species of large lemur (Propithecus sp., Indri indri). In addition to the polymorphism detected earlier, in some species at least two other polymorphic variants involving substitutions at positions 180 and 277 were identified (Jacobs et al., 2017). The results from the totality of the genetic work shows some of the diurnal strepsirrhines could well be trichromats.
Nature and Utility of Primate Color Vision
The discussion thus far has focused on research conducted on opsin genes and cone photopigments. Many of the works cited have offered inferences about color vision. In fact, claims about color vision often appear in the titles of these papers. Actual studies of primate color vision—those that entail behavioral assessments—have been much less frequent. These studies provide the indispensable link relating structure to function and thus are critical for furthering progress toward understanding the nature and utility of primate color vision.
A vast majority of what has been learned about human color vision comes from careful laboratory experiments where viewing conditions can be rigidly controlled. For mostly practical reasons, there have been only a relative handful of analogous experiments on nonhuman primates (for reviews see Jacobs, 2008; Kelber & Jacobs, 2016). These studies provide a standard for directly linking photopigment complement to basic features of color vision.
A step beyond these basic laboratory experiments involves the exploitation of what are referred to as seminatural conditions, those involving circumstances in which stimuli in behavioral tests are crafted to mimic natural scenes. One example is a study by Smith, Buchanan-Smith, Surridge, Osorio, and Mundy (2003) that measured the spectral reflectance properties of fruits and foliage from the natural habitats of polymorphic tamarin monkeys (Saguinus sp.). These measurements were then used to produce spectral replicas of ripe and unripe fruits displayed in artificial foliage, and monkeys were tested to see how quickly and efficiently they learned to “harvest” the ripe fruits. Trichromatic tamarins were found to outperform their dichromatic conspecifics in this task, suggesting they enjoy a visual advantage linked to their differences in color vision dimensionality. There have been similar studies that contrasted performances of animals with different color vision phenotypes with various results. Some found an obvious trichromatic advantage but others failed to do so (for reviews see Jacobs, 2015; Kawamura & Melin, 2017).
Models for Color Discrimination
To evaluate and predict experimental outcomes, researchers have increasingly turned to the use of formal models of color discrimination. These are based on the spectral properties of relevant stimuli married to assumptions of how the visual system analyzes such signals to yield color vision. Although several models incorporate explicit assumptions about the processing of color signals within the visual nervous system, the most popular one assumes that threshold color discriminations are based solely on differences in stimulus chromaticity as tied to the number of photoreceptor classes, their spectral sensitivity, and their noise properties (Vorobyev & Osorio, 1998).
The receptor noise model successfully accounts for laboratory results from tests of spectral sensitivity and color vision in a number of species (Renoult, Kelber, & Schaefer, 2017; Vorobyev & Osorio, 1998). Recently this model has increasingly been applied to viewing circumstances often far removed from those present in controlled laboratory tests. Olsson, Lind, and Kelber (2017) outlines stimulus parameters and visual system properties where it may be unrealistic to assume color discrimination is entirely limited by receptor noise. The conclusion that emerges from this paper and the appended discussion is that models of color discrimination can prove useful in evaluating animal color vision, but the predictions derived from them needs to be grounded in the context of results from direct behavioral tests.
A touchstone for studies of primate color vision is understanding how this capacity is employed in natural environments. There is a large body of literature on the multiple uses to which humans exploit color cues (Elliott et al., 2015). For nonhuman primates, it has been variously suggested that color vision provides critical information for the detection and evaluation of potential food sources, of conspecifics, and of predators. The discovery of widespread polymorphisms in New World monkeys provides an attractive laboratory in which to evaluate these possibilities. A typical field study involves spectrophotometric measurements of potential visual targets (e.g., fruits, foliage, arthropods, predators), of the backgrounds in which these targets are embedded, and of the ambient illumination. These are then coupled with observations designed to understand how monkeys of different cone phenotypes interact with such targets.
One popular idea to explain the maintenance of opsin gene polymorphisms across many generations in platyrrhine monkeys is that the trichromatic individuals enjoy an advantage. Field studies of monkeys provide mixed support for this idea (i.e., some studies detect trichromatic superiority, but others do not; Kawamura & Melin, 2017; Kelber & Jacobs, 2016). It now seems likely that presence or absence of trichromatic superiority is task and situation dependent. For example, studies of Cebus monkeys found that although trichromats were superior to dichromats in foraging for small patches of colorful flowers (Hogan, Fedigan, Hiramatsu, Kawamura, & Melin, 2018), there are no differences across phenotypes for feeding rates on figs (Melin et al., 2009). Yet in some viewing circumstances a dichromatic advantage has been be detected (Melin, Fedigan, Hiramatsu, Sendall, & Kawamura, 2007). The conclusion from several such studies is that natural habitats offer a plethora of viewing conditions and behavioral opportunities, and that whereas trichromatic color vision can be shown to be a positive asset in some circumstances, in others dichromats suffer no disadvantage and may even enjoy an advantage.
There is a balanced polymorphism of L/M opsin genes in New World monkeys and a continuing question is what factor(s) operate to maintain that balance. A study by Fedigan, Melin, Addicott, and Kawamura (2014) sought to shed light on that question. They note that of the mechanisms typically hypothesized to support balanced polymorphisms (frequency dependent selection, niche divergence, mutual benefit of association), only one, heterozygous advantage (heterosis), specifically predicts enhanced fitness in trichromats as opposed to dichromats. To test this, they examined life histories of a group of female Cebus monkeys from a study site in Costa Rico gathered over a 26-year period. They found no differences in three fitness measures (fertility rates, offspring, and maternal survival) for dichromats and trichromats, which suggests that heterozygous advantage is not operating to maintain the polymorphism and thus other mechanisms must be at play. Curiously, a somewhat similar set of measurements made on Cebus monkeys at a different study site (in Argentina) does find evidence that trichromats have higher fitness (Green, 2014). These conflicting results suggest that heterozygous advantage may not have been critical for maintaining a balanced color vision polymorphism in the environmental niches of some polymorphic platyrrhines, but was centrally important in others.
I thank Gabe Luna for help with the illustrations.
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