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Many of these reported cases of phenotypic convergence involve pigmentation (see Hubbard et al., 2010), notably in the color of skin (Miller et al., 2007; Gross et al., 2009), fur (Hoekstra et al., 2006; Kingsley et al., 2009; Steiner et al., 2009), or plumage (Mundy, 2005). In primates, blue iris pigmentation has been documented in four different lineages. In humans (Homo sapiens), the prevalence of the trait increases with latitude from 24 to 55% in European populations (Zanetti et al., 1996; Laeng et al., 2007); it has also been observed in populations with European admixture (Frudakis et al., 2007). In Japanese macaques (Macaca fuscata), which are endemic to the broad-leaved deciduous and evergreen forests of Japan (Oi, 2002; Abe et al., 2005), blue or intermediate iris color has been observed at frequencies of 12 to 19% in colonies on Shodoshima and Kyushu islands (Yamagiwa, 1979; Zhang and Watanabe, 2007). Blue irises have also been reported in the brown spider monkey (Ateles hybridus, formerly Ateles belzebuth hybridus; Hernandez-Camacho and Cooper, 1976; Konstant et al., 1985) and closely related Colombian black spider monkey (Ateles geoffroyi or fusciceps, subspecies rufiventris; Hernandez-Camacho and Cooper, 1976; Defler et al., 2004), which inhabit evergreen, semi-deciduous, and montane seasonal forests in Colombia, Panama, and Venezuela (Mondolfi and Eisenberg, 1979; Defler et al., 2004). Although the prevalence of this trait in these species has not been extensively documented, approximately 13% of a population of brown spider monkeys in north central Colombia has blue irises (R. Rimbach and A. Link, personal communication). In contrast to these other species, all blue-eyed black lemurs (Eulemur flavifrons, formerly Eulemur macaco flavifrons) have blue irises, whereas in the most closely related species, the black lemur (Eulemur macaco, formerly Eulemur macaco macaco), all individuals have brown irises (Mittermeier et al., 2006). These sister species inhabit primary and secondary tropical sub-humid forests in a narrow range in northwestern Madagascar (Rabarivola et al., 1991; Andrianjakarivelo, 2004; Randriatahina and Rabarivola, 2004) and hybridize across part of this range (Rabarivola et al., 1991). Given that almost all other primates have brown or yellow irises (Kobayashi and Kohshima, 2001), blue iris pigmentation can be inferred to be a derived trait that has arisen independently on these lineages.
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Beyond these broad strokes, the extent of iris pigmentation variation within and between species has not been characterized. In particular, it is not yet clear whether the reported blue irises represent the same phenotype in all species. Demonstrating such similarity is important, as if the derived phenotypes were different, we would anticipate the involvement of distinct genetic loci. Thus, mapping the traits would not provide additional information with regard to evolutionary constraint. Quantitative measures of iris pigmentation variation, recently demonstrated to be associated with genetic variation in humans (Liu et al., 2010a; Edwards et al., 2012), provide a way of evaluating phenotypic similarity across species.
Our understanding of the genetic basis of blue iris pigmentation in humans can inform hypotheses regarding the genetic basis in other primates. In humans, several coding sequence mutations and deletions of coding regions in OCA2 cause oculocutaneous albinism, or severely reduced pigmentation of the hair, skin, and irises (Manga and Orlow, 1999; Oetting and King, 1999), whereas regulatory SNP rs12913832 has a more moderate influence on hair and skin phenotypes (Sulem et al., 2007; Branicki et al., 2009). If dramatic pigmentation reduction in skin or fur were deleterious in other primates, we may expect blue irises to evolve via regulatory mutations in these species as well. Notably, SNP rs12913832 lies within a stretch of 410 bp demonstrating strong conservation among mammals; thus, this region is a strong candidate for variants with the capacity to influence OCA2 expression. Bradley et al. (2009) sequenced 166 bp of the orthologous region and found no fixed differences between the two lemur species. They identified one variant that was polymorphic within the blue-eyed black lemurs but not the black lemurs sequenced, a pattern that could be suggestive of this variant or a linked site contributing to pigmentation differences.
Several lines of evidence support the idea that blue irises have fitness effects in humans. The rarity of observation of the phenotype in nature, in combination with observed deleterious pleiotropic consequences in humans (Eagle Jr, 1994; Imesch et al., 1997; Metallinos et al., 1998; Santschi et al., 1998; Yang et al., 1998; Smith et al., 2000; Pingault et al., 2010) and domesticated animals (Juraschko et al., 2003; Geigy et al., 2007; Hauswirth et al., 2012), suggests that some benefit would be required to overcome purifying selection against these pleiotropic effects. Population genetic evidence also supports recent positive selection at the locus responsible for the majority of the phenotypic variation in humans (Voight et al., 2006; Donnelly et al., 2012; Yang et al., 2012). Although the mechanism driving this population genetic signature is unclear, direct selection for blue irises to improve short wavelength perception (Bornstein, 1973; Laeng et al., 2007), selection for light skin pigmentation to increase vitamin D absorption (see, e.g., Jablonski and Chaplin, 2000; Parra, 2007), and sexual selection (Darwin, 1871; Diamond, 1992; Aoki, 2002; Frost, 2006; Laeng et al., 2007) may have played a part.
Independent plots for each species or group showing quantitative phenotypic variation in the CIE L*a*b* color system, with color representing visible color (as in Fig. 1). (A) Japanese macaques, (B) blue-eyed black lemurs and black lemurs, (C) brown spider monkeys, and (D) humans.
Our comparison of the phenotypic variation across species suggests hypotheses about the genetic basis of blue irises in Japanese macaques and blue-eyed black lemurs. In humans, iris color varies continuously (e.g., Frudakis et al., 2007; Edwards et al., 2012); however, our perception of this spectrum of variation has led us to categorize iris color into discrete classes: e.g., blue, green, and brown (Kayser et al., 2008; Liu et al., 2010a). The genetic basis of iris color variation in humans reflects both these perceived discrete categories (>80% of the variation in blue vs. brown can be explained by a single mutation) and the underlying continuous nature of the phenotype (several additional loci with more modest effects have been identified; see, e.g., Sulem et al., 2007; Liu et al., 2010a). In Japanese macaques, as in humans, iris color variation is continuous in CIE L*a*b* space (Fig. 2A). This may suggest that one or a few loci have strong effect, producing the perceived blue/brown distinction, with additional genetic or environmental modifiers generating a continuous spectrum between these extremes. In contrast, phenotypic variation is discontinuous between the photographed blue-eyed black lemurs and black lemurs; one or more fixed genetic differences contributing to iris color differences between species could explain this discontinuity. Alternatively, the derived trait may result from a combination of changes in several genes, thus allowing specific variants to segregate within blue-eyed black lemurs. Additional phenotypic data from brown spider monkey populations might enable predictions about the genetic architecture of iris color variation in this species as well.
The observation of a variant just upstream of the human causal variant in the sample of blue-eyed black lemurs, but not the sample of black lemurs, raises the possibility that this variant or one linked to it influences iris pigmentation. Although this variant cannot produce blue irises on its own, it could do so in combination with variation at other loci. Such a complex genetic basis for iris pigmentation could explain the intermediate phenotype observed in hybrids between blue-eyed black lemurs and black lemurs (Meyers et al., 1989; Rabarivola et al., 1991).
In humans, the pigmentation of the iris varies from light brown to black, depending on the concentration of melanin in the iris pigment epithelium (located on the back of the iris), the melanin content within the iris stroma (located at the front of the iris), and the cellular density of the stroma.[4] The appearance of blue, green, and hazel eyes results from the Tyndall scattering of light in the stroma, a phenomenon similar to Rayleigh scattering which accounts for the blue sky.[5] Neither blue nor green pigments are present in the human iris or ocular fluid.[3][6] This is an example of structural color, which depends on the lighting conditions, especially for lighter-colored eyes.
Normal eye colors range from the darkest shades of brown to the lightest tints of blue.[13] To meet the need for standardized classification, at once simple yet detailed enough for research purposes, Seddon et al. developed a graded system based on the predominant iris color and the amount of brown or yellow pigment present.[22] There are three pigment colors that determine, depending on their proportion, the outward appearance of the iris, along with structural color. Green irises, for example, have some yellow and the blue structural color. Brown irises contain more or less melanin. Some eyes have a dark ring around the iris, called a limbal ring.
Most newborn babies who have European ancestry have light-colored eyes. As the child develops, melanocytes (cells found within the iris of human eyes, as well as skin and hair follicles) slowly begin to produce melanin. Because melanocyte cells continually produce pigment, in theory eye color can be changed. Adult eye color is usually established between 3 and 6 months of age, though this can be later.[26] Observing the iris of an infant from the side using only transmitted light with no reflection from the back of the iris, it is possible to detect the presence or absence of low levels of melanin. An iris that appears blue under this method of observation is more likely to remain blue as the infant ages. An iris that appears golden contains some melanin even at this early age and is likely to turn from blue to green or brown as the infant ages. 2ff7e9595c
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