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Eye color in domestic pigeons (Columba livia). Wild-type individuals exhibit a pigmented yellow iris, while pearl-eye mutants (controlled by a recessive allele) show unpigmented eyes. The yellow coloration of wild-type pigeons is due to the deposition of pterins in the pigmented epithelium of the iris. Photo credits: P. M. Araújo. https://doi.org/10.1371/journal.pgen.1009404.g001
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Birds exhibit striking variation in eye color that arises from interactions between specialized pigment cells named chromatophores. The types of chromatophores present in the avian iris are lacking from the integument of birds or mammals, but are remarkably similar to those found in the skin of ectothermic vertebrates. To investigate molecular mech...
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Context 1
... good model to investigate the molecular determinants of eye color variation and pigment cell evolution in birds is the domestic pigeon (Columba livia , Fig 1). Pigeons typically have eyes exhibiting a range of yellow and red hues, which arise from the deposition of pterin pigments in the anterior surface of the iris combined with strong vascularization [15]. ...
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... with less than 50% of the positions passing filters were excluded. A range of additional window sizes were used (5kb, 50kb, 100kb, and 200kb), but the results remained qualitatively unchanged with the top candidate region consistently emerging as the top outlier region. ...
Citations
... Those photophores could be a source of molecules that contribute to luminescence and possibly bill fluorescence. Although pterin pigments account for the coloration of the iris in some birds (Oliphant 1987), the genes involved are not expressed in the integument of birds or mammals (Andrade et al. 2021). The fluorescent pigment must be supplied via the circulating blood plasma to the cells that secrete the bill pigment, and we suspect it is sequestered or metabolized from prey. ...
Crested auklets (Aethia cristatella) are colonial seabirds with brilliant orange bills during the breeding season. We characterized the bill pigment with spectroscopy methods (resonance Raman, fluorescence, absorbance). We excluded carotenoids as a possible chromophore and showed that the pigment most closely resembles pterins. Like pterins the bill pigment fluoresces, and it occurred in two phenotypes that may differ geographically, perhaps due to environmental heterogeneity. The pigment is unique in the Genus Aethia, and its spectra did not match any known molecule. The UV-Vis absorbance spectrum of the bill pigment overlaps with the extracted pigment of euphausiids, a favored food of crested auklets. A color preference associated with prey may have favored characteristics of the crested auklet's accessory bill plates. Crest size, a signal of dominance, tended to correlate positively with highest fluorescence in the single-band phenotype. Brighter bills may function in self-advertisement and verify the status signal of the crest ornament. We tested for a behavioral preference using identical decoys that differed only in bill fluorescence. Crested auklets approached models with fluorescent bills at a higher frequency. In cases where sex of crested auklets was known, males responded at a higher frequency to fluorescent bills, but females did not. In an evolutionary context, bill fluorescence could have conferred an advantage in social interactions, e.g., in dimly lit rock crevices. Bill brightness and color may communicate success in foraging and may function as an honest signal of mate quality.
... The exact role of SPR in drosopterin synthesis in lizards is unclear, since this link has not been established in insect models. In another recent finding, the membrane transporter SLC2A11B was shown to regulate pterin-based eye colour in xanthophore-like iris pigment cells of pigeons [147][148][149]. Interestingly, this gene is also involved in xanthophore differentiation in medaka [150], but the exact cellular and molecular links between these two cases (pigment uptake versus cell differentiation) are unknown. ...
Pterins are one of the major sources of bright coloration in animals. They are produced endogenously, participate in vital physiological processes and serve a variety of signalling functions. Despite their ubiquity in nature, pterin-based pigmentation has received little attention when compared to other major pigment classes. Here, we summarize major aspects relating to pterin pigmentation in animals, from its long history of research to recent genomic studies on the molecular mechanisms underlying its evolution. We argue that pterins have intermediate characteristics (endogenously produced, typically bright) between two well-studied pigment types, melanins (endogenously produced, typically cryptic) and carotenoids (dietary uptake, typically bright), providing unique opportunities to address general questions about the biology of coloration, from the mechanisms that determine how different types of pigmentation evolve to discussions on honest signalling hypotheses. Crucial gaps persist in our knowledge on the molecular basis underlying the production and deposition of pterins. We thus highlight the need for functional studies on systems amenable for laboratory manipulation, but also on systems that exhibit natural variation in pterin pigmentation. The wealth of potential model species, coupled with recent technological and analytical advances, make this a promising time to advance research on pterin-based pigmentation in animals.
... Mutant domestic pigeons with white "pearl" irises lack yellow pteridine pigments in their irises. Two studies independently showed that a nonsense mutation in the gene SLC2A11B is likely responsible for pearl-colored irises (Si et al. 2020;Andrade et al. 2021), consistent with its role in xanthophore (yellow chromatophore) differentiation in fishes (Kimura et al. 2014). Si et al. (2020) also identified a fixed frameshift mutation in SLC2A11B in several cormorant species, which have characteristically blue structurally colored irises that lack pteridine or purine pigments. ...
... Si et al. (2020) also identified a fixed frameshift mutation in SLC2A11B in several cormorant species, which have characteristically blue structurally colored irises that lack pteridine or purine pigments. The apparent link between SLC2A11B in pteridine synthesis in bird irises and in fish xanthophores suggests that birds may share a molecular mechanism for pteridine coloration with ectothermic animals (Andrade et al. 2021), consistent with the hypothesis that avian irises represent evolutionary refugia for chromatophores (Oliphant et al. 1992). Therefore, known pigmentation genes in fish may be good candidate genes for further investigation of iris coloration in birds (Andrade et al. 2021). ...
... The apparent link between SLC2A11B in pteridine synthesis in bird irises and in fish xanthophores suggests that birds may share a molecular mechanism for pteridine coloration with ectothermic animals (Andrade et al. 2021), consistent with the hypothesis that avian irises represent evolutionary refugia for chromatophores (Oliphant et al. 1992). Therefore, known pigmentation genes in fish may be good candidate genes for further investigation of iris coloration in birds (Andrade et al. 2021). Despite some progress on the genetics of carotenoid-and chromatophore-based bare part coloration, the genetic basis of the collagen fiber arrays that produce structurally colored skin, bills, feet, and legs is completely unknown. ...
The colorful phenotypes of birds have long provided rich source material for evolutionary biologists. Avian plumage, beaks, skin, and eggs—which exhibit a stunning range of cryptic and conspicuous forms—inspired early work on adaptive coloration. More recently, avian color has fueled discoveries on the physiological, developmental, and—increasingly—genetic mechanisms responsible for phenotypic variation. The relative ease with which avian color traits can be quantified has made birds an attractive system for uncovering links between phenotype and genotype. Accordingly, the field of avian coloration genetics is burgeoning. In this review, we highlight recent advances and emerging questions associated with the genetic underpinnings of bird color. We start by describing breakthroughs related to 2 pigment classes: carotenoids that produce red, yellow, and orange in most birds and psittacofulvins that produce similar colors in parrots. We then discuss structural colors, which are produced by the interaction of light with nanoscale materials and greatly extend the plumage palette. Structural color genetics remain understudied—but this paradigm is changing. We next explore how colors that arise from interactions among pigmentary and structural mechanisms may be controlled by genes that are co-expressed, co-expressed or co-regulated. We also identify opportunities to investigate genes mediating within-feather micropatterning and the coloration of bare parts and eggs. We conclude by spotlighting 2 research areas—mechanistic links between color vision and color production, and speciation—that have been invigorated by genetic insights, a trend likely to continue as new genomic approaches are applied to non-model species.
Birds display a rainbow of eye colours, but this trait has been little studied compared with plumage coloration. Avian eye colour variation occurs at all phylogenetic scales: it can be conserved throughout whole families or vary within one species, yet the evolutionary importance of this eye colour variation is under‐studied. Here, we summarize knowledge of the causes of eye colour variation at three primary levels: mechanistic, genetic and evolutionary. Mechanistically, we show that avian iris pigments include melanin and carotenoids, which also play major roles in plumage colour, as well as purines and pteridines, which are often found as pigments in non‐avian taxa. Genetically, we survey classical breeding studies and recent genomic work on domestic birds that have identified potential ‘eye colour genes’, including one associated with pteridine pigmentation in pigeons. Finally, from an evolutionary standpoint, we present and discuss several hypotheses explaining the adaptive significance of eye colour variation. Many of these hypotheses suggest that bird eye colour plays an important role in intraspecific signalling, particularly as an indicator of age or mate quality, although the importance of eye colour may differ between species and few evolutionary hypotheses have been directly tested. We suggest that future studies of avian eye colour should consider all three levels, including broad‐scale iris pigment analyses across bird species, genome sequencing studies to identify loci associated with eye colour variation, and behavioural experiments and comparative phylogenetic analyses to test adaptive hypotheses. By examining these proximate and ultimate causes of eye colour variation in birds, we hope that our review will encourage future research to understand the ecological and evolutionary significance of this striking avian trait.
Mutations in the HERC2 and OCA2 genes have the potential to affect pigment deposition and alter feather color in birds. Therefore, in this study, we evaluated HERC2-OCA2 gene locus polymorphisms in Korean and Beijing white quails using RNA-Seq and KASP technology. The expression levels of HERC2 and OCA2 mRNA in skin tissues were analyzed using RT-qPCR. Ten single nucleotide polymorphisms were identified by RNA-Seq, of which three (n.117627564T>A, n.117674275T>G, n.117686226A>C) exhibited significant association with feather color in quail. The expression of OCA2 mRNA was significantly lower in the skin of Beijing white quails than that in the skin of Korean quails. These results suggested that variants in HERC2-OCA2 intergenic region could influence the expression of OCA2, which may underlie diluted feather color in the Beijing white quail.
Repeated phenotypic patterns among populations undergoing parallel evolution in similar environments provide support for the deterministic role of natural selection. Epigenetic modifications can mediate plastic and evolved phenotypic responses to environmental change and might make important contributions to parallel adaptation. While many studies have explored the genetic basis of repeated phenotypic divergence, the role of epigenetic processes during parallel adaptation remains unclear. The parallel evolution of freshwater ecotypes of threespine stickleback fish (Gasterosteus aculeatus) following colonization of thousands of lakes and streams from the ocean is a classic example of parallel phenotypic and genotypic adaptation. To investigate epigenetic modifications during parallel adaptation of threespine stickleback, we reanalyzed three independent datasets that investigated DNA methylation variation between marine and freshwater ecotypes. Although we found widespread methylation differentiation between ecotypes, there was no significant tendency for CpG sites associated with repeated methylation differentiation across studies to be parallel versus non‐parallel. To next investigate the role of plastic versus evolved changes in methylation during freshwater adaptation, we explored if CpG sites exhibiting methylation plasticity during salinity change were more likely to also show evolutionary divergence in methylation between ecotypes. The directions of divergence between ecotypes were generally in the opposite direction to those observed for plasticity when ecotypes were challenged with non‐native salinity conditions, suggesting that most plastic responses are likely to be maladaptive during colonization of new environments. Finally, we found a greater number of CpG sites showing evolved changes when ancestral marine ecotypes are acclimated to freshwater environments, whereas plastic changes predominate when derived freshwater ecotypes transition back to their ancestral marine environments. These findings provide evidence for an epigenetic contribution to parallel adaptation and demonstrate the contrasting roles of plastic and evolved methylation differences during adaptation to new environments.
The iris of the eye shows striking color variation across vertebrate species, and may play important roles in crypsis and communication. The domestic pigeon (Columba livia) has three common iris colors, orange, pearl (white), and bull (dark brown), segregating in a single species, thereby providing a unique opportunity to identify the genetic basis of iris coloration. We used comparative genomics and genetic mapping in laboratory crosses to identify two candidate genes that control variation in iris color in domestic pigeons. We identified a nonsense mutation in the solute carrier SLC2A11B that is shared among all pigeons with pearl eye color, and a locus associated with bull eye color that includes EDNRB2, a gene involved in neural crest migration and pigment development. However, bull eye is likely controlled by a heterogeneous collection of alleles across pigeon breeds. We also found that the EDNRB2 region is associated with regionalized plumage depigmentation (piebalding). Our study identifies two candidate genes for eye colors variation, and establishes a genetic link between iris and plumage color, two traits that vary widely in the evolution of birds and other vertebrates.
