Primate color vision: A comparative perspective

Abstract Thirty years ago virtually everything known about primate color vision derived from psychophysical studies of normal and color-defective humans and from physiological investigations of the visual system of the macaque monkey, the most popular of human surrogates for this purpose. The years since have witnessed much progress toward the goal of understanding this remarkable feature of primate vision. Among many advances, investigations focused on naturally occurring variations in color vision in a wide range of nonhuman primate species have proven to be particularly valuable. Results from such studies have been central to our expanding understanding of the interrelationships between opsin genes, cone photopigments, neural organization, and color vision. This work is also yielding valuable insights into the evolution of color vision.

[1]  N. Pierce Origin of Species , 1914, Nature.

[2]  G. L. Walls,et al.  The Vertebrate Eye and Its Adaptive Radiation , 1943 .

[3]  H. E. Roaf The Vertebrate Eye and its Adaptive Radiation , 1943, Nature.

[4]  R. H. Post,et al.  Population differences in red and green color vision deficiency: a review, and a query on selection relaxation. , 1962, Eugenics quarterly.

[5]  G. Wald,et al.  Visual Pigments in Human and Monkey Retinas , 1963, Nature.

[6]  W. B. Marks,et al.  Visual Pigments of Single Primate Cones , 1964, Science.

[7]  V C Smith,et al.  Large-field trichromacy in protanopes and deuteranopes. , 1977, Journal of the Optical Society of America.

[8]  J. Mollon,et al.  Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[9]  Robert Fletcher,et al.  DEFECTIVE COLOUR VISION FUNDAMENTALS, DIAGNOSIS AND MANAGEMENT , 1985 .

[10]  J. Nathans,et al.  Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. , 1986, Science.

[11]  L. Peichl,et al.  Topography of cones and rods in the tree shrew retina , 1989, The Journal of comparative neurology.

[12]  R. Martin Primate origins and evolution , 1990 .

[13]  J D Mollon,et al.  Photosensitive and photostable pigments in the retinae of Old World monkeys. , 1991, The Journal of experimental biology.

[14]  G H Jacobs,et al.  Spectral tuning of pigments underlying red-green color vision. , 1991, Science.

[15]  B. Boycott,et al.  Functional architecture of the mammalian retina. , 1991, Physiological reviews.

[16]  Donald J. Zack,et al.  A locus control region adjacent to the human red and green visual pigment genes , 1992, Neuron.

[17]  G. H. Jacobs,et al.  Photopigments underlying color vision in ringtail lemurs (Lemur catta) and brown lemurs (Eulemur fulvus) , 1993, American journal of primatology.

[18]  E. Costa,et al.  Glutamate-activated currents in outside-out patches from spiny versus aspiny hilar neurons of rat hippocampal slices , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  G. H. Jacobs THE DISTRIBUTION AND NATURE OF COLOUR VISION AMONG THE MAMMALS , 1993, Biological reviews of the Cambridge Philosophical Society.

[20]  G. H. Jacobs,et al.  Photopigments and color vision in the nocturnal monkey,Aotus , 1993, Vision Research.

[21]  D. Dacey The mosaic of midget ganglion cells in the human retina , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  John D. Mollon,et al.  Structure and evolution of the polymorphic photopigment gene of the marmoset , 1993, Vision Research.

[23]  Barry B. Lee,et al.  The 'blue-on' opponent pathway in primate retina originates from a distinct bistratified ganglion cell type , 1994, Nature.

[24]  Bb Lee,et al.  Visual responses in the lateral geniculate nucleus of dichromatic and trichromatic marmosets (Callithrix jacchus) , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  G. H. Jacobs,et al.  Mutations in S-cone pigment genes and the absence of colour vision in two species of nocturnal primate , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  G. H. Jacobs Primate photopigments and primate color vision. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Paul R. Martin,et al.  Comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat, and the marmoset Callithrix jacchus , 1996, The Journal of comparative neurology.

[28]  Jay Neitz,et al.  Trichromatic colour vision in New World monkeys , 1996, Nature.

[29]  J. Neitz,et al.  Recent evolution of uniform trichromacy in a New World monkey , 1998, Vision Research.

[30]  G H Jacobs,et al.  The topography of rod and cone photoreceptors in the retina of the ground squirrel , 1998, Visual Neuroscience.

[31]  Vivien A Casagrande,et al.  Morphology of P and M retinal ganglion cells of the bush baby , 1998, Vision Research.

[32]  Barry B. Lee,et al.  Comparative retinal physiology in anthropoids , 1998, Vision Research.

[33]  G H Jacobs,et al.  Transgenic mice expressing a functional human photopigment. , 1998, Investigative ophthalmology & visual science.

[34]  G. H. Jacobs,et al.  A perspective on color vision in platyrrhine monkeys , 1998, Vision Research.

[35]  D. Hewett‐Emmett,et al.  Origins and antiquity of X-linked triallelic color vision systems in New World monkeys. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Paul R. Martin,et al.  Colour processing in the primate retina: recent progress , 1998, The Journal of physiology.

[37]  G. Fowler,et al.  Rod influence on hue-scaling functions , 1998, Vision Research.

[38]  H. Komatsu,et al.  Dichromatism in macaque monkeys. , 1999, Nature.

[39]  G. H. Jacobs,et al.  Uniformity of colour vision in Old World monkeys , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[40]  B. B. Lee,et al.  Ganglion cells of a short-wavelength-sensitive cone pathway in New World monkeys: Morphology and physiology , 1999, Visual Neuroscience.

[41]  B. Boycott,et al.  Parallel processing in the mammalian retina: the Proctor Lecture. , 1999, Investigative ophthalmology & visual science.

[42]  G H Jacobs,et al.  Human Cone Pigment Expressed in Transgenic Mice Yields Altered Vision , 1999, The Journal of Neuroscience.

[43]  J. Mollon,et al.  The evolution of trichromatic color vision by opsin gene duplication in New World and Old World primates. , 1999, Genome research.

[44]  S. Yokoyama,et al.  The molecular genetics of red and green color vision in mammals. , 1999, Genetics.

[45]  A. Hendrickson,et al.  Nocturnal tarsier retina has both short and long/medium‐wavelength cones in an unusual topography , 2000, The Journal of comparative neurology.

[46]  P. Lennie,et al.  Fine Structure of Parvocellular Receptive Fields in the Primate Fovea Revealed by Laser Interferometry , 2000, The Journal of Neuroscience.

[47]  S. Yokoyama Molecular evolution of vertebrate visual pigments , 2000, Progress in Retinal and Eye Research.

[48]  David J. Calkins,et al.  Seeing with S cones , 2001, Progress in Retinal and Eye Research.

[49]  D. Macdonald New encyclopedia of mammals , 2001 .

[50]  J. Schmitz,et al.  SINE insertions in cladistic analyses and the phylogenetic affiliations of Tarsius bancanus to other primates. , 2001, Genetics.

[51]  G. H. Jacobs,et al.  The prevalence of defective color vision in Old World monkeys and apes , 2001 .

[52]  R. Masland The fundamental plan of the retina , 2001, Nature Neuroscience.

[53]  C. Ross,et al.  Evolution of activity patterns and chromatic vision in primates: morphometrics, genetics and cladistics. , 2001, Journal of human evolution.

[54]  J. Mollon,et al.  Fruits, foliage and the evolution of primate colour vision. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[55]  L. J. Anthony The New Encyclopedia of Mammals , 2002 .

[56]  L. Beazley,et al.  Trichromacy in Australian Marsupials , 2002, Current Biology.

[57]  Jeremy Nathans,et al.  Role of a locus control region in the mutually exclusive expression of human red and green cone pigment genes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[58]  G. H. Jacobs,et al.  Opsin gene and photopigment polymorphism in a prosimian primate , 2002, Vision Research.

[59]  N. Mundy,et al.  Trans‐specific evolution of opsin alleles and the maintenance of trichromatic colour vision in Callitrichine primates , 2002, Molecular ecology.

[60]  S. Kawamura,et al.  Ancestral Loss of Short Wave-Sensitive Cone Visual Pigment in Lorisiform Prosimians, Contrasting with Its Strict Conservation in Other Prosimians , 2004, Journal of Molecular Evolution.

[61]  E. Fernández‐Duque Influences of moonlight, ambient temperature, and food availability on the diurnal and nocturnal activity of owl monkeys (Aotus azarai) , 2003, Behavioral Ecology and Sociobiology.

[62]  J. Mollon 1 – The Origins of Modern Color Science , 2003 .

[63]  Jianzhi Zhang Evolution by gene duplication: an update , 2003 .

[64]  Gerald H. Jacobs,et al.  Genetically engineered mice with an additional class of cone photoreceptors: Implications for the evolution of color vision , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[65]  S. Shevell The Science of Color , 2003 .

[66]  J. Pokorny,et al.  3 – Color Matching and Color Discrimination , 2003 .

[67]  Barry B. Lee,et al.  Morphology and physiology of primate M- and P-cells. , 2004, Progress in brain research.

[68]  A. E. Trezíse,et al.  The origins of colour vision in vertebrates , 2004, Clinical & experimental optometry.

[69]  M. Vorobyev Ecology and evolution of primate colour vision , 2004, Clinical & experimental optometry.

[70]  Callum F. Ross,et al.  Anthropoid origins : new visions , 2004 .

[71]  Barry B. Lee,et al.  Paths to colour in the retina , 2004, Clinical & experimental optometry.

[72]  J. Bowmaker,et al.  Divergent mechanisms for the tuning of shortwave sensitive visual pigments in vertebrates , 2004, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[73]  M. Vorobyev,et al.  Detection of Fruit and the Selection of Primate Visual Pigments for Color Vision , 2004, The American Naturalist.

[74]  L. Chalupa,et al.  The visual neurosciences , 2004 .

[75]  Heinz Wässle,et al.  Parallel processing in the mammalian retina , 2004, Nature Reviews Neuroscience.

[76]  Xijun Ni,et al.  A euprimate skull from the early Eocene of China , 2004, Nature.

[77]  N. Dominy Color as an Indicator of Food Quality to Anthropoid Primates: Ecological Evidence and an Evolutionary Scenario , 2004 .

[78]  Barry B. Lee,et al.  Alouatta trichromatic color vision – single–unit recording from retinal ganglion cells and microspectrophotometry. , 2004 .

[79]  H. Wässle,et al.  The Primordial, Blue-Cone Color System of the Mouse Retina , 2005, The Journal of Neuroscience.

[80]  Y. Attia,et al.  Basal Anthropoids from Egypt and the Antiquity of Africa's Higher Primate Radiation , 2005, Science.

[81]  G. H. Jacobs,et al.  Polymorphic New World monkeys with more than three M/L cone types. , 2005, Journal of the Optical Society of America. A, Optics, image science, and vision.

[82]  Joel Pokorny,et al.  Matching rod percepts with cone stimuli , 2004, Vision Research.

[83]  William R. Mathew,et al.  Color as a Science , 2005 .

[84]  M. Tachibana,et al.  Generation of Knock-in Mice Carrying Third Cones with Spectral Sensitivity Different from S and L Cones , 2005, Zoological science.

[85]  Wen-Hsiung Li,et al.  Evidence from opsin genes rejects nocturnality in ancestral primates. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[86]  M. McCall,et al.  Stimulus size and intensity alter fundamental receptive-field properties of mouse retinal ganglion cells in vivo , 2005, Visual Neuroscience.

[87]  L. Peichl Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[88]  Almut Kelber,et al.  Nocturnal colour vision – not as rare as we might think , 2006, Journal of Experimental Biology.

[89]  R. Martin,et al.  The Evolutionary and Ecological Context of Primate Vision , 2006 .

[90]  Gerald H Jacobs,et al.  L and M cone proportions in polymorphic New World monkeys , 2006, Visual Neuroscience.

[91]  G. H. Jacobs,et al.  The Genetics and Evolution of Primate Visual Pigments , 2006 .

[92]  Nathan M. Young,et al.  Primate molecular divergence dates. , 2006, Molecular phylogenetics and evolution.

[93]  I. Tattersall The Concept of Cathemerality: History and Definition , 2006, Folia Primatologica.

[94]  J. Kremers The primate visual system : a comparative approach , 2006 .

[95]  K. Nekaris,et al.  A Re-Evaluation of the Role of Vision in the Activity and Communication of Nocturnal Primates , 2006, Folia Primatologica.

[96]  Behavioural evidence for marsupial trichromacy , 2006, Current Biology.

[97]  S. DeVries,et al.  Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina , 2006, Nature Neuroscience.

[98]  S. Tavaré,et al.  Primate Origins: Implications of a Cretaceous Ancestry , 2007, Folia Primatologica.

[99]  D. Hunt,et al.  Avian Visual Pigments: Characteristics, Spectral Tuning, and Evolution , 2007, The American Naturalist.

[100]  Ian J. Corfe MAMMALS FROM THE AGE OF DINOSAURS—ORIGINS, EVOLUTION, AND STRUCTURE , 2007 .

[101]  Kate E. Jones,et al.  The delayed rise of present-day mammals , 1990, Nature.

[102]  Gerald H Jacobs,et al.  Mutational changes in S‐cone opsin genes common to both nocturnal and cathemeral Aotus monkeys , 2007, American journal of primatology.

[103]  G. Perry,et al.  Signatures of functional constraint at aye-aye opsin genes: the potential of adaptive color vision in a nocturnal primate. , 2007, Molecular biology and evolution.

[104]  B. Danforth Bees , 2007, Current Biology.

[105]  G. H. Jacobs,et al.  Emergence of Novel Color Vision in Mice Engineered to Express a Human Cone Photopigment , 2007, Science.

[106]  P. Lennie,et al.  The machinery of colour vision , 2007, Nature Reviews Neuroscience.

[107]  Callum F. Ross,et al.  The Role of Vision in the Origin and Evolution of Primates , 2007 .

[108]  G. H. Jacobs New World Monkeys and Color , 2007, International Journal of Primatology.

[109]  Carlos G Schrago,et al.  On the time scale of New World primate diversification. , 2007, American journal of physical anthropology.

[110]  J. Bowmaker Evolution of vertebrate visual pigments , 2008, Vision Research.

[111]  M. A. Macneil,et al.  Biocytin wide‐field bipolar cells in rabbit retina selectively contact blue cones , 2008, The Journal of comparative neurology.

[112]  David Hunt Molecular evolution of colour vision in primates , 2010 .