Skip to main content
Log in

The genetic and evolutionary basis of colour variation in vertebrates

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Variation in pigmentation is one of the most conspicuous phenotypic traits in vertebrates. Although mammals show less variation in body pigmentation than other vertebrate groups, the genetics of colour determination and variation is best understood for them. More than 150 genes have been identified that influence pigmentation, and in many cases, the cause for variation in pigmentation has been identified down to the underlying nucleotide changes. These studies show that while some genes are often responsible for deviating pigmentation, similar or almost identical phenotypes even in the same species may be due to mutations in different genes. In this review we will first discuss the current knowledge about the genes and their functions underlying the biochemical pathways that determine pigmentation and then give examples where the mutations responsible for colour variation have been determined. Finally, we will discuss potential evolutionary causes for and consequences of differences in pigmentation between individuals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Otaki JM (2008) Physiologically induced color-pattern changes in butterfly wings: mechanistic and evolutionary implications. J Insect Physiol 54:1099–1112

    PubMed  CAS  Google Scholar 

  2. Parchem RJ, Perry MW, Patel NH (2007) Patterns on the insect wing. Curr Opin Genet Dev 17:300–308

    PubMed  CAS  Google Scholar 

  3. Papa R, Martin A, Reed RD (2008) Genomic hotspots of adaptation in butterfly wing pattern evolution. Curr Opin Genet Dev 18:559–564

    PubMed  CAS  Google Scholar 

  4. O’Grady PM, DeSalle R (2000) How the fruit fly changed (some of) its spots. Curr Biol 10:R75–R77

    PubMed  Google Scholar 

  5. Oetting WS, Austin LM, Bennett DC (2009) Color genes: European Society for Pigment Cell Research. http://www.espcr.org/micemut/

  6. Simon JD, Peles D, Wakamatsu K, Ito S (2009) Current challenges in understanding melanogenesis: bridging chemistry, biological control, morphology, and function. Pigment Cell Melanoma Res 22:563–579

    PubMed  CAS  Google Scholar 

  7. Barsh G, Cotsarelis G (2007) How hair gets its pigment. Cell 130:779–781

    PubMed  CAS  Google Scholar 

  8. Weiner L, Han R, Scicchitano BM, Li J, Hasegawa K, Grossi M, Lee D, Brissette JL (2007) Dedicated epithelial recipient cells determine pigmentation patterns. Cell 130:932–942

    PubMed  CAS  Google Scholar 

  9. Sturm RA (2009) Molecular genetics of human pigmentation diversity. Hum Mol Genet 18:R9–R17

    PubMed  CAS  Google Scholar 

  10. Ito S, Wakamatsu K (2008) Chemistry of mixed melanogenesis: pivotal roles of dopaquinone. Photochem Photobiol 84:582–592

    PubMed  CAS  Google Scholar 

  11. Slominski A, Tobin DJ, Shibahara S, Wortsman J (2004) Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol Rev 84:1155–1228

    PubMed  CAS  Google Scholar 

  12. Schallreuter KU (2007) Advances in melanocyte basic science research. Dermatol Clin 25:283–291 vii

    PubMed  CAS  Google Scholar 

  13. Cone RD, Lu D, Koppula S, Vage DI, Klungland H, Boston B, Chen W, Orth DN, Pouton C, Kesterson RA (1996) The melanocortin receptors: agonists, antagonists, and the hormonal control of pigmentation. Recent Prog Horm Res 51:287–317 discussion 318

    PubMed  CAS  Google Scholar 

  14. Fredriksson R, Schioth HB (2005) The repertoire of G-protein-coupled receptors in fully sequenced genomes. Mol Pharmacol 67:1414–1425

    PubMed  CAS  Google Scholar 

  15. Rees JL (2003) Genetics of hair and skin color. Annu Rev Genet 37:67–90

    PubMed  CAS  Google Scholar 

  16. Ha T, Naysmith L, Waterston K, Oh C, Weller R, Rees JL (2003) Defining the quantitative contribution of the melanocortin 1 receptor (MC1R) to variation in pigmentary phenotype. Ann N Y Acad Sci 994:339–347

    PubMed  CAS  Google Scholar 

  17. Kerje S, Lind J, Schutz K, Jensen P, Andersson L (2003) Melanocortin 1-receptor (MC1R) mutations are associated with plumage colour in chicken. Anim Genet 34:241–248

    PubMed  CAS  Google Scholar 

  18. Robbins LS, Nadeau JH, Johnson KR, Kelly MA, Roselli-Rehfuss L, Baack E, Mountjoy KG, Cone RD (1993) Pigmentation phenotypes of variant extension locus alleles result from point mutations that alter MSH receptor function. Cell 72:827–834

    PubMed  CAS  Google Scholar 

  19. Kijas JM, Wales R, Tornsten A, Chardon P, Moller M, Andersson L (1998) Melanocortin receptor 1 (MC1R) mutations and coat color in pigs. Genetics 150:1177–1185

    PubMed  CAS  Google Scholar 

  20. Vage DI, Klungland H, Lu D, Cone RD (1999) Molecular and pharmacological characterization of dominant black coat color in sheep. Mamm Genome 10:39–43

    PubMed  CAS  Google Scholar 

  21. Vage DI, Lu D, Klungland H, Lien S, Adalsteinsson S, Cone RD (1997) A non-epistatic interaction of agouti and extension in the fox, Vulpes vulpes. Nat Genet 15:311–315

    PubMed  CAS  Google Scholar 

  22. Kazius J, Wurdinger K, van Iterson M, Kok J, Back T, Ijzerman AP (2008) GPCR NaVa database: natural variants in human G protein-coupled receptors. Hum Mutat 29:39–44

    PubMed  CAS  Google Scholar 

  23. Kanetsky PA, Rebbeck TR, Hummer AJ, Panossian S, Armstrong BK, Kricker A, Marrett LD, Millikan RC, Gruber SB, Culver HA, Zanetti R, Gallagher RP, Dwyer T, Busam K, From L, Mujumdar U, Wilcox H, Begg CB, Berwick M (2006) Population-based study of natural variation in the melanocortin-1 receptor gene and melanoma. Cancer Res 66:9330–9337

    PubMed  CAS  Google Scholar 

  24. Lefkowitz RJ, Cotecchia S, Samama P, Costa T (1993) Constitutive activity of receptors coupled to guanine nucleotide regulatory proteins. Trends Pharmacol Sci 14:303–307

    PubMed  CAS  Google Scholar 

  25. Haitina T, Ringholm A, Kelly J, Mundy NI, Schioth HB (2007) High diversity in functional properties of melanocortin 1 receptor (MC1R) in divergent primate species is more strongly associated with phylogeny than coat color. Mol Biol Evol 24:2001–2008

    PubMed  CAS  Google Scholar 

  26. Schaffer JV, Bolognia JL (2001) The melanocortin-1 receptor: red hair and beyond. Arch Dermatol 137:1477–1485

    PubMed  CAS  Google Scholar 

  27. Norris BJ, Whan VA (2008) A gene duplication affecting expression of the ovine ASIP gene is responsible for white and black sheep. Genome Res 18:1282–1293

    PubMed  CAS  Google Scholar 

  28. Linnen CR, Kingsley EP, Jensen JD, Hoekstra HE (2009) On the origin and spread of an adaptive allele in deer mice. Science 325:1095–1098

    PubMed  CAS  Google Scholar 

  29. Kingsley EP, Manceau M, Wiley CD, Hoekstra HE (2009) Melanism in peromyscus is caused by independent mutations in agouti. PLoS One 4:e6435

    PubMed  Google Scholar 

  30. Slominski A, Plonka PM, Pisarchik A, Smart JL, Tolle V, Wortsman J, Low MJ (2005) Preservation of eumelanin hair pigmentation in proopiomelanocortin-deficient mice on a nonagouti (a/a) genetic background. Endocrinology 146:1245–1253

    PubMed  CAS  Google Scholar 

  31. Candille SI, Kaelin CB, Cattanach BM, Yu B, Thompson DA, Nix MA, Kerns JA, Schmutz SM, Millhauser GL, Barsh GS (2007) A -defensin mutation causes black coat color in domestic dogs. Science 318:1418–1423

    PubMed  CAS  Google Scholar 

  32. Anderson TM, vonHoldt BM, Candille SI, Musiani M, Greco C, Stahler,DR, Smith DW, Padhukasahasram B, Randi E, Leonard JA, Bustamante CD, Ostrander EA, Tang H, Wayne RK, Barsh GS (2009) Molecular and evolutionary history of melanism in North American gray wolves. Science 323:1339–1343

    PubMed  CAS  Google Scholar 

  33. Bassi MT, Schiaffino MV, Renieri A, De Nigris F, Galli L, Bruttini M, Gebbia M, Bergen AA, Lewis RA, Ballabio A (1995) Cloning of the gene for ocular albinism type 1 from the distal short arm of the X chromosome. Nat Genet 10:13–19

    PubMed  CAS  Google Scholar 

  34. Lopez VM, Decatur CL, Stamer WD, Lynch RM, McKay BS (2008) l-DOPA is an endogenous ligand for OA1. PLoS Biol 6:e236

    PubMed  Google Scholar 

  35. Schiaffino MV, Bassi MT, Galli L, Renieri A, Bruttini M, De Nigris F, Bergen AA, Charles SJ, Yates JR, Meindl A et al (1995) Analysis of the OA1 gene reveals mutations in only one-third of patients with X-linked ocular albinism. Hum Mol Genet 4:2319–2325

    PubMed  CAS  Google Scholar 

  36. Incerti B, Cortese K, Pizzigoni A, Surace EM, Varani S, Coppola M, Jeffery G, Seeliger M, Jaissle G, Bennett DC, Marigo V, Schiaffino MV, Tacchetti C, Ballabio A (2000) Oa1 knock-out: new insights on the pathogenesis of ocular albinism type 1. Hum Mol Genet 9:2781–2788

    PubMed  CAS  Google Scholar 

  37. Protas ME, Hersey C, Kochanek D, Zhou Y, Wilkens H, Jeffery WR, Zon LI, Borowsky R, Tabin CJ (2006) Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nat Genet 38:107–111

    PubMed  CAS  Google Scholar 

  38. Fukamachi S, Shimada A, Shima A (2001) Mutations in the gene encoding B, a novel transporter protein, reduce melanin content in medaka. Nat Genet 28:381–385

    PubMed  CAS  Google Scholar 

  39. Haase B, Brooks SA, Schlumbaum A, Azor PJ, Bailey E, Alaeddine F, Mevissen M, Burger D, Poncet PA, Rieder S, Leeb T (2007) Allelic heterogeneity at the equine KIT locus in dominant white (W) horses. PLoS Genet 3:e195

    PubMed  Google Scholar 

  40. Geissler EN, Ryan MA, Housman DE (1988) The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene. Cell 55:185–192

    PubMed  CAS  Google Scholar 

  41. Albert FW, Carlborg O, Plyusnina I, Besnier F, Hedwig D, Lautenschläger S, Lorenz D, McIntosh J, Neumann C, Richter H, Zeising C, Kozhemyakina R, Shchepina O, Kratzsch J, Trut L, Teupser D, Thiery J, Schöneberg T, Andersson L, Päbo S (2009) Genetic architecture of tameness in a rat model of animal domestication. Genetics 182:541–554

    PubMed  Google Scholar 

  42. Johansson Moller M, Chaudhary R, Hellmen E, Hoyheim B, Chowdhary B, Andersson L (1996) Pigs with the dominant white coat color phenotype carry a duplication of the KIT gene encoding the mast/stem cell growth factor receptor. Mamm Genome 7:822–830

    PubMed  CAS  Google Scholar 

  43. Goda M, Fujii R (1998) The blue coloration of the common surgeonfish, Paracanthurus hepatus-II: color revelation and color changes. Zool Sci 15:323–333

    PubMed  CAS  Google Scholar 

  44. Nachman MW, Hoekstra HE, D’Agostino SL (2003) The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad Sci USA 100:5268–5273

    PubMed  CAS  Google Scholar 

  45. Hoekstra HE, Nachman MW (2003) Different genes underlie adaptive melanism in different populations of rock pocket mice. Mol Ecol 12:1185–1194

    PubMed  CAS  Google Scholar 

  46. Hoekstra HE, Hirschmann RJ, Bundey RA, Insel PA, Crossland JP (2006) A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313:101–104

    PubMed  CAS  Google Scholar 

  47. Rosenblum EB, Hoekstra HE, Nachman MW (2004) Adaptive reptile color variation and the evolution of the Mc1r gene. Evolution 58:1794–1808

    PubMed  CAS  Google Scholar 

  48. Dice L, Blossom PM (1937) Studies of mammalian ecology in southwestern North America, with special attention to the colors of desert mammals. Publ Carnegie Inst Washington 485:1–25

    Google Scholar 

  49. Kaufmann DW (1974) Adaptive coloration in Peromyscus polionotus: experimental selection by owls. J Mammal 55:271–283

    Google Scholar 

  50. Rosenblum EB, Römpler H, Schöneberg T, Hoekstra HE (2010) Molecular and functional basis of phenotypic convergence in white lizards at White Sands. Proc Natl Acad Sci USA 107:2113–2117

    PubMed  CAS  Google Scholar 

  51. Price AC, Weadick CJ, Shim J, Rodd FH (2008) Pigments, patterns, and fish behavior. Zebrafish 5:297–307

    PubMed  Google Scholar 

  52. Marshall NJ, Vorobyev M (2003) The design of color signals and color vision in fishes. In: Collin SP, Marshall NJ (eds) Sensory Processing in Aquatic Environments. Springer, New York, pp 194–222

    Google Scholar 

  53. Leonard JA, Wayne RK, Wheeler J, Valadez R, Guillen S, Vila C (2002) Ancient DNA evidence for old world origin of new world dogs. Science 298:1613–1616

    PubMed  CAS  Google Scholar 

  54. Olendorf R, Rodd FH, Punzalan D, Houde AE, Hurt C, Reznick DN, Hughes KA (2006) Frequency-dependent survival in natural guppy populations. Nature 441:633–636

    PubMed  CAS  Google Scholar 

  55. Eakley AL, Houde AE (2004) Possible role of female discrimination against ‘redundant’ males in the evolution of colour pattern polymorphism in guppies. Proc Biol Sci 271(Suppl 5):S299–S301

    PubMed  Google Scholar 

  56. Zajitschek SR, Brooks RC (2008) Distinguishing the effects of familiarity, relatedness, and color pattern rarity on attractiveness and measuring their effects on sexual selection in guppies (Poecilia reticulata). Am Nat 172:843–854

    PubMed  Google Scholar 

  57. Pierotti MER, Seehausen O (2006) Male mating preferences pre-date the origin of a female trait polymorphism in an incipient species complex of Lake Victoria cichlids. J Evol Biol 20:240–248

    Google Scholar 

  58. Morris MR, Rios-Cardenas O, Scarlett Tudor M (2006) Larger swordtail females prefer asymmetrical males. Biol Lett 2:8–11

    PubMed  Google Scholar 

  59. Roulin A (2004) The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol Rev Camb Philos Soc 79:815–848

    PubMed  Google Scholar 

  60. Marshall HD, Ritland K (2002) Genetic diversity and differentiation of Kermode bear populations. Mol Ecol 11:685–697

    PubMed  CAS  Google Scholar 

  61. Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HD, Miyagi R, van der Sluijs I, Schneider MV, Maan ME, Tachida H, Imai H, Okada N (2008) Speciation through sensory drive in cichlid fish. Nature 455:620–626

    PubMed  CAS  Google Scholar 

  62. Schluter D, Price T (1993) Honesty, perception and population divergence in sexually selected traits. Proc Biol Sci 253:117–122

    PubMed  CAS  Google Scholar 

  63. Boughman JW (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944–948

    PubMed  CAS  Google Scholar 

  64. Genner MJ, Nichols P, Carvalho GR, Robinson RL, Shaw PW, Turner GF (2007) Reproductive isolation among deep-water cichlid fishes of Lake Malawi differing in monochromatic male breeding dress. Mol Ecol 16:651–662

    PubMed  Google Scholar 

  65. Rodd FH, Hughes KA, Grether GF, Baril CT (2002) A possible non-sexual origin of mate preference: are male guppies mimicking fruit? Proc Biol Sci 269:475–481

    PubMed  Google Scholar 

  66. Barber I, Arnott SA, Braithwaite VA, Andrew J, Huntingford FA (2001) Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proc Biol Sci 268:71–76

    PubMed  CAS  Google Scholar 

  67. Milinski M, Bakker TCM (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330–333

    Google Scholar 

  68. Bakker TCM and Mundwiler B (1994). Female mate choice and male red colouration in a natural three-spined stickleback (Gasterosteus aculeatus) population. Behav Ecol 5:74–80

    Google Scholar 

  69. Grether GF, Kolluru GR, Rodd FH, de la Cerda J, Shimazaki K (2005) Carotenoid availability affects the development of a colour-based mate preference and the sensory bias to which it is genetically linked. Proc Biol Sci 272:2181–2188

    PubMed  Google Scholar 

  70. Candolin U, Salesto T, Evers M (2007) Changed environmental conditions weaken sexual selection in sticklebacks. J Evol Biol 20:233–239

    PubMed  CAS  Google Scholar 

  71. Jarvenpaa M, Lindstrom K (2004) Water turbidity by algal blooms causes mating system breakdown in a shallow-water fish, the sand goby Pomatoschistus minutus. Proc Biol Sci 271:2361–2365

    PubMed  Google Scholar 

  72. Pauers MJ, Kapfer JM, Fendos CE, Berg CS (2008) Aggressive biases towards similarly coloured males in Lake Malawi cichlid fishes. Biol Lett 4:156–159

    PubMed  Google Scholar 

  73. Seehausen O, Schluter D (2004) Male-male competition and nuptial-colour displacement as a diversifying force in Lake Victoria cichlid fishes. Proc Biol Sci 271:1345–1353

    PubMed  Google Scholar 

  74. Turner GF, Burrows MT (1995) A model of sympatric speciation by sexual selection. Proc R Soc Lond B 260:287–292

    Google Scholar 

  75. Mountjoy KG, Robbins LS, Mortrud MT, Cone RD (1992) The cloning of a family of genes that encode the melanocortin receptors. Science 257:1248–1251

    PubMed  CAS  Google Scholar 

  76. Hoekstra HE (2006) Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity 97:222–234

    PubMed  CAS  Google Scholar 

  77. Garcia-Borron JC, Sanchez-Laorden BL, Jimenez-Cervantes C (2005) Melanocortin-1 receptor structure and functional regulation. Pigment Cell Res 18:393–410

    PubMed  CAS  Google Scholar 

  78. Bultman SJ, Michaud EJ, Woychik RP (1992) Molecular characterization of the mouse agouti locus. Cell 71:1195–1204

    PubMed  CAS  Google Scholar 

  79. Cerda-Reverter JM, Haitina T, Schioth HB, Peter RE (2005) Gene structure of the goldfish agouti-signaling protein: a putative role in the dorsal-ventral pigment pattern of fish. Endocrinology 146:1597–1610

    PubMed  CAS  Google Scholar 

  80. Klovins J, Schioth HB (2005) Agouti-related proteins (AGRPs) and agouti-signaling peptide (ASIP) in fish and chicken. Ann N Y Acad Sci 1040:363–367

    PubMed  CAS  Google Scholar 

  81. Selz Y, Braasch I, Hoffmann C, Schmidt C, Schultheis C, Schartl M, Volff JN (2007) Evolution of melanocortin receptors in teleost fish: the melanocortin type 1 receptor. Gene 401:114–122

    PubMed  CAS  Google Scholar 

  82. Nocka K, Majumder S, Chabot B, Ray P, Cervone M, Bernstein A, Besmer P (1989) Expression of c-kit gene products in known cellular targets of W mutations in normal and W mutant mice–evidence for an impaired c-kit kinase in mutant mice. Genes Dev 3:816–826

    PubMed  CAS  Google Scholar 

  83. Bagnara JT, Hadley ME (1973) Chromatophores and colour change: the comparative physiology of animal pigmentation. Prentice Hall, New Jersey

    Google Scholar 

  84. Metz JR, Peters JJ, Flik G (2006) Molecular biology and physiology of the melanocortin system in fish: a review. Gen Comp Endocrinol 148:150–162

    PubMed  CAS  Google Scholar 

  85. Klovins J, Haitina T, Fridmanis D, Kilianova Z, Kapa I, Fredriksson R, Gallo-Payet N, Schioth HB (2004) The melanocortin system in Fugu: determination of POMC/AGRP/MCR gene repertoire and synteny, as well as pharmacology and anatomical distribution of the MCRs. Mol Biol Evol 21:563–579

    PubMed  CAS  Google Scholar 

  86. van der Salm AL, Metz JR, Bonga SE, Flik G (2005) Alpha-MSH, the melanocortin-1 receptor and background adaptation in the Mozambique tilapia, Oreochromis mossambicus. Gen Comp Endocrinol 144:140–149

    PubMed  Google Scholar 

  87. Gross JB, Borowsky R, Tabin CJ (2009) A novel role for Mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax mexicanus. PLoS Genet 5:e1000326

    PubMed  Google Scholar 

  88. Ollmann MM, Lamoreux ML, Wilson BD, Barsh GS (1998) Interaction of Agouti protein with the melanocortin 1 receptor in vitro and in vivo. Genes Dev 12:316–330

    PubMed  CAS  Google Scholar 

  89. Barsh G, Gunn T, He L, Schlossman S, Duke-Cohan J (2000) Biochemical and genetic studies of pigment-type switching. Pigment Cell Res 13(Suppl 8):48–53

    PubMed  Google Scholar 

  90. Pointer MA, Mundy NI (2008) Testing whether macroevolution follows microevolution: are colour differences among swans (Cygnus) attributable to variation at the MCIR locus? BMC Evol Biol 8:249

    PubMed  Google Scholar 

  91. Baiao PC, Schreiber E, Parker PG (2007) The genetic basis of the plumage polymorphism in red-footed boobies (Sula sula): a melanocortin-1 receptor (MC1R) analysis. J Hered 98:287–292

    PubMed  CAS  Google Scholar 

  92. Nadeau NJ, Mundy NI, Gourichon D, Minvielle F (2007) Association of a single-nucleotide substitution in TYRP1 with roux in Japanese quail (Coturnix japonica). Anim Genet 38:609–613

    Article  PubMed  CAS  Google Scholar 

  93. Nadeau NJ, Minvielle F, Mundy NI (2006) Association of a Glu92Lys substitution in MC1R with extended brown in Japanese quail (Coturnix japonica). Anim Genet 37:287–289

    PubMed  CAS  Google Scholar 

  94. Doucet SM, Shawkey MD, Rathburn MK, Mays HL Jr, Montgomerie R (2004) Concordant evolution of plumage colour, feather microstructure and a melanocortin receptor gene between mainland and island populations of a fairy-wren. Proc Biol Sci 271:1663–1670

    PubMed  CAS  Google Scholar 

  95. Theron E, Hawkins K, Bermingham E, Ricklefs RE, Mundy NI (2001) The molecular basis of an avian plumage polymorphism in the wild: a melanocortin-1-receptor point mutation is perfectly associated with the melanic plumage morph of the bananaquit, Coereba flaveola. Curr Biol 11:550–557

    PubMed  CAS  Google Scholar 

  96. Mundy NI, Badcock NS, Hart T, Scribner K, Janssen K, Nadeau NJ (2004) Conserved genetic basis of a quantitative plumage trait involved in mate choice. Science 303:1870–1873

    PubMed  CAS  Google Scholar 

  97. Cooke F, Finney GH, Rockwell RF (1976) Assortative mating in lesser snow geese (Anser caerulescens). Behav Genet 6:127–140

    PubMed  CAS  Google Scholar 

  98. Phillips RA, Furness RW (1998) Polymorphism, mating preferences and sexual selection in the Arctic skua. J Zool 245:245–252

    Google Scholar 

  99. Nadeau NJ, Burke T, Mundy NI (2007) Evolution of an avian pigmentation gene correlates with a measure of sexual selection. Proc Biol Sci 274:1807–1813

    PubMed  CAS  Google Scholar 

  100. Eizirik E, Yuhki N, Johnson WE, Menotti-Raymond M, Hannah SS, O’Brien SJ (2003) Molecular genetics and evolution of melanism in the cat family. Curr Biol 13:448–453

    PubMed  CAS  Google Scholar 

  101. Römpler H, Rohland N, Lalueza-Fox C, Willerslev E, Kuznetsova T, Rabeder G, Bertranpetit J, Schöneberg T, Hofreiter M (2006) Nuclear gene indicates coat-color polymorphism in mammoths. Science 313:62

    PubMed  Google Scholar 

  102. Duffy DL, Zhao ZZ, Sturm RA, Hayward NK, Martin NG, Montgomery GW (2010) Multiple pigmentation gene polymorphisms account for a substantial proportion of risk of cutaneous malignant melanoma. J Invest Dermatol 130:520–528

    PubMed  CAS  Google Scholar 

  103. Han J, Kraft P, Nan H, Guo Q, Chen C, Qureshi A, Hankinson SE, Hu FB, Duffy DL, Zhao ZZ, Martin NG, Montgomery GW, Hayward NK, Thomas G, Hoover RN, Chanock S, Hunter DJ (2008) A genome-wide association study identifies novel alleles associated with hair color and skin pigmentation. PLoS Genet 4:e1000074

    PubMed  Google Scholar 

  104. Sulem P, Gudbjartsson DF, Stacey SN, Helgason A, Rafnar T, Magnusson KP, Manolescu A, Karason A, Palsson A, Thorleifsson G, Jakobsdottir M, Steinberg S, Palsson S, Jonasson F, Sigurgeirsson B, Thorisdottir K, Ragnarsson R, Benediktsdottir KR, Aben KK, Kiemeney LA, Olafsson JH, Gulcher J, Kong A, Thorsteinsdottir U, Stefansson K (2007) Genetic determinants of hair, eye and skin pigmentation in Europeans. Nat Genet 39:1443–1452

    PubMed  CAS  Google Scholar 

  105. Sturm RA, Frudakis TN (2004) Eye colour: portals into pigmentation genes and ancestry. Trends Genet 20:327–332

    PubMed  CAS  Google Scholar 

  106. Eiberg H, Troelsen J, Nielsen M, Mikkelsen A, Mengel-From J, Kjaer KW, Hansen L (2008) Blue eye color in humans may be caused by a perfectly associated founder mutation in a regulatory element located within the HERC2 gene inhibiting OCA2 expression. Hum Genet 123:177–187

    PubMed  CAS  Google Scholar 

  107. Schöneberg T, Schulz A, Biebermann H, Hermsdorf T, Rompler H, Sangkuhl K (2004) Mutant G-protein-coupled receptors as a cause of human diseases. Pharmacol Ther 104:173–206

    PubMed  Google Scholar 

  108. Flanagan N, Healy E, Ray A, Philips S, Todd C, Jackson IJ, Birch-Machin MA, Rees JL (2000) Pleiotropic effects of the melanocortin 1 receptor (MC1R) gene on human pigmentation. Hum Mol Genet 9:2531–2537

    PubMed  CAS  Google Scholar 

  109. Harding RM, Healy E, Ray AJ, Ellis NS, Flanagan N, Todd C, Dixon C, Sajantila A, Jackson IJ, Birch-Machin MA, Rees JL (2000) Evidence for variable selective pressures at MC1R. Am J Hum Genet 66:1351–1361

    PubMed  CAS  Google Scholar 

  110. Meyle KD, Guldberg P (2009) Genetic risk factors for melanoma. Hum Genet 126:499–510

    PubMed  CAS  Google Scholar 

  111. Ibrahim N, Haluska FG (2009) Molecular pathogenesis of cutaneous melanocytic neoplasms. Annu Rev Pathol 4:551–579

    PubMed  CAS  Google Scholar 

  112. Landi MT, Bauer J, Pfeiffer RM, Elder DE, Hulley B, Minghetti P, Calista D, Kanetsky PA, Pinkel D, Bastian BC (2006) MC1R germline variants confer risk for BRAF-mutant melanoma. Science 313:521–522

    PubMed  CAS  Google Scholar 

  113. Lalueza-Fox C, Römpler H, Caramelli D, Stäubert C, Catalano G, Hughes D, Rohland N, Pilli E, Longo L, Condemi S, de la Rasilla M, Fortea J, Rosas A, Stoneking M, Schöneberg T, Bertranpetit J, Hofreiter M (2007) A melanocortin 1 receptor allele suggests varying pigmentation among Neanderthals. Science 318:1453–1455

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Brenda Bradley, Hopi Hoekstra and Ole Seehausen for providing pictures and Regina Querner for help with the figure design. This work was funded by the DFG, the Max Planck Society and the University of York.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael Hofreiter.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hofreiter, M., Schöneberg, T. The genetic and evolutionary basis of colour variation in vertebrates. Cell. Mol. Life Sci. 67, 2591–2603 (2010). https://doi.org/10.1007/s00018-010-0333-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-010-0333-7

Keywords

Navigation