1932

Abstract

Vertebrate pigment patterns are diverse and fascinating adult traits that allow animals to recognize conspecifics, attract mates, and avoid predators. Pigment patterns in fish are among the most amenable traits for studying the cellular basis of adult form, as the cells that produce diverse patterns are readily visible in the skin during development. The genetic basis of pigment pattern development has been most studied in the zebrafish, . Zebrafish adults have alternating dark and light horizontal stripes, resulting from the precise arrangement of three main classes of pigment cells: black melanophores, yellow xanthophores, and iridescent iridophores. The coordination of adult pigment cell lineage specification and differentiation with specific cellular interactions and morphogenetic behaviors is necessary for stripe development. Besides providing a nice example of pattern formation responsible for an adult trait of zebrafish, stripe-forming mechanisms also provide a conceptual framework for posing testable hypotheses about pattern diversification more broadly. Here, we summarize what is known about lineages and molecular interactions required for pattern formation in zebrafish, we review some of what is known about pattern diversification in , and we speculate on how patterns in more distant teleosts may have evolved to produce a stunningly diverse array of patterns in nature.

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2019-12-03
2024-10-12
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Literature Cited

  1. 1. 
    Adameyko I, Lallemend F, Aquino JB, Pereira JA, Topilko P et al. 2009. Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell 139:366–79
    [Google Scholar]
  2. 2. 
    Bagnara JT. 1982. Development of the spot pattern in the leopard frog. J. Exp. Zool. 224:283–87
    [Google Scholar]
  3. 3. 
    Barrett RDH, Laurent S, Mallarino R, Pfeifer SP, Xu CCY et al. 2019. Linking a mutation to survival in wild mice. Science 363:499–504
    [Google Scholar]
  4. 4. 
    Booth CL. 1990. Evolutionary significance of ontogenetic colour change in animals. Biol. J. Linn. Soc. 40:125–63
    [Google Scholar]
  5. 5. 
    Brodie ED III 1992. Correlational selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution 46:1284–98
    [Google Scholar]
  6. 6. 
    Budi EH, Patterson LB, Parichy DM 2008. Embryonic requirements for ErbB signaling in neural crest development and adult pigment pattern formation. Development 135:2603–14
    [Google Scholar]
  7. 7. 
    Budi EH, Patterson LB, Parichy DM 2011. Post-embryonic nerve-associated precursors to adult pigment cells: genetic requirements and dynamics of morphogenesis and differentiation. PLOS Genet 7:e1002044
    [Google Scholar]
  8. 8. 
    Cal L, Suarez-Bregua P, Cerdá-Reverter JM, Braasch I, Rotllant J 2017. Fish pigmentation and the melanocortin system. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 211:26–33
    [Google Scholar]
  9. 9. 
    Camargo-Sosa K, Colanesi S, Müller J, Schulte-Merker S, Stemple D et al. 2019. Endothelin receptor Aa regulates proliferation and differentiation of Erb-dependent pigment progenitors in zebrafish. PLOS Genet 15:e1007941
    [Google Scholar]
  10. 10. 
    Carvalho FR, Fernandes AR, Cancela ML, Gavaia PJ 2017. Improved regeneration and de novo bone formation in a diabetic zebrafish model treated with paricalcitol and cinacalcet. Wound Repair Regen 25:432–42
    [Google Scholar]
  11. 11. 
    Ceinos RM, Guillot R, Kelsh RN, Cerdá-Reverter JM, Rotllant J 2015. Pigment patterns in adult fish result from superimposition of two largely independent pigmentation mechanisms. Pigment Cell Melanoma Res 28:196–209
    [Google Scholar]
  12. 12. 
    Culumber ZW. 2014. Pigmentation in Xiphophorus: an emerging system in ecological and evolutionary genetics. Zebrafish 11:57–70
    [Google Scholar]
  13. 13. 
    Curran K, Lister JA, Kunkel GR, Prendergast A, Parichy DM, Raible DW 2010. Interplay between Foxd3 and Mitf regulates cell fate plasticity in the zebrafish neural crest. Dev. Biol. 344:107–18
    [Google Scholar]
  14. 14. 
    Dalle Nogare D, Chitnis AB 2017. Self-organizing spots get under your skin. PLOS Biol 15:e2004412
    [Google Scholar]
  15. 15. 
    Debbache J, Parfejevs V, Sommer L 2018. Cre-driver lines used for genetic fate mapping of neural crest cells in the mouse: an overview. Genesis 56:e23105
    [Google Scholar]
  16. 16. 
    Dooley CM. 2014. On the origin and differentiation of melanophores in zebrafish, Danio rerio PhD diss. Univ. Tübingen, Ger.
    [Google Scholar]
  17. 17. 
    Dooley CM, Mongera A, Walderich B, Nüsslein-Volhard C 2013. On the embryonic origin of adult melanophores: the role of ErbB and Kit signalling in establishing melanophore stem cells in zebrafish. Development 140:1003–13
    [Google Scholar]
  18. 18. 
    Dorsky RI, Raible DW, Moon RT 2000. Direct regulation of nacre, a zebrafish MITF homolog required for pigment cell formation, by the Wnt pathway. Genes Dev 14:158–62
    [Google Scholar]
  19. 19. 
    Dushane GP. 1934. The origin of pigment cells in Amphibia. Science 80:620–21
    [Google Scholar]
  20. 20. 
    Endler JA. 1983. Natural and sexual selection on color patterns in poeciliid fishes. Environ. Biol. Fishes 9:173–90
    [Google Scholar]
  21. 21. 
    Engeszer RE, Da Barbiano LA, Ryan MJ, Parichy DM 2007. Timing and plasticity of shoaling behaviour in the zebrafish, Danio rerio. Anim. Behav. 74:1269–75
    [Google Scholar]
  22. 22. 
    Engeszer RE, Ryan MJ, Parichy DM 2004. Learned social preference in zebrafish. Curr. Biol. 14:881–84
    [Google Scholar]
  23. 23. 
    Engeszer RE, Wang G, Ryan MJ, Parichy DM 2008. Sex-specific perceptual spaces for a vertebrate basal social aggregative behavior. PNAS 105:929–33
    [Google Scholar]
  24. 24. 
    Eom DS, Bain EJ, Patterson LB, Grout ME, Parichy DM 2015. Long-distance communication by specialized cellular projections during pigment pattern development and evolution. eLife 4:e12401
    [Google Scholar]
  25. 25. 
    Eom DS, Inoue S, Patterson LB, Gordon TN, Slingwine R et al. 2012. Melanophore migration and survival during zebrafish adult pigment stripe development require the immunoglobulin superfamily adhesion molecule Igsf11. PLOS Genet 8:e1002899
    [Google Scholar]
  26. 26. 
    Eom DS, Parichy DM. 2017. A macrophage relay for long-distance signaling during postembryonic tissue remodeling. Science 355:1317–20
    [Google Scholar]
  27. 27. 
    Fadeev A, Krauss J, Frohnhöfer H-G, Irion U, Nüsslein-Volhard C 2015. Tight Junction Protein 1a regulates pigment cell organisation during zebrafish colour patterning. eLife 4:e06545
    [Google Scholar]
  28. 28. 
    Fadeev A, Krauss J, Singh AP, Nüsslein-Volhard C 2016. Zebrafish leucocyte tyrosine kinase controls iridophore establishment, proliferation and survival. Pigment Cell Melanoma Res 29:284–96
    [Google Scholar]
  29. 29. 
    Fadeev A, Mendoza-Garcia P, Irion U, Guan J, Pfeifer K et al. 2018. ALKALs are in vivo ligands for ALK family receptor tyrosine kinases in the neural crest and derived cells. PNAS 115:E630–38
    [Google Scholar]
  30. 30. 
    Frohnhöfer H-G, Geiger-Rudolph S, Pattky M, Meixner M, Huhn C et al. 2016. Spermidine, but not spermine, is essential for pigment pattern formation in zebrafish. Biol. Open 5:736–44
    [Google Scholar]
  31. 31. 
    Frohnhöfer H-G, Krauss J, Maischein HM, Nüsslein-Volhard C 2013. Iridophores and their interactions with other chromatophores are required for stripe formation in zebrafish. Development 140:2997–3007
    [Google Scholar]
  32. 32. 
    Fukamachi S, Sugimoto M, Mitani H, Shima A 2004. Somatolactin selectively regulates proliferation and morphogenesis of neural-crest derived pigment cells in medaka. PNAS 101:10661–66
    [Google Scholar]
  33. 33. 
    Fukamachi S, Wakamatsu Y, Mitani H 2006. Medaka double mutants for color interfere and leucophore free: characterization of the xanthophore–somatolactin relationship using the leucophore free gene. Dev. Genes Evol. 216:152–57
    [Google Scholar]
  34. 34. 
    Fukamachi S, Yada T, Meyer A, Kinoshita M 2009. Effects of constitutive expression of somatolactin alpha on skin pigmentation in medaka. Gene 442:81–87
    [Google Scholar]
  35. 35. 
    Gans C, Northcutt RG. 1983. Neural crest and the origin of vertebrates: a new head. Science 220:268–74
    [Google Scholar]
  36. 36. 
    Geissler EN, Ryan MA, Housman DE 1988. The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene. Cell 55:185–92
    [Google Scholar]
  37. 37. 
    Greenhill ER, Rocco A, Vibert L, Nikaido M, Kelsh RN 2011. An iterative genetic and dynamical modelling approach identifies novel features of the gene regulatory network underlying melanocyte development. PLOS Genet 7:e1002265
    [Google Scholar]
  38. 38. 
    Hamada H, Watanabe M, Lau HE, Nishida T, Hasegawa T et al. 2014. Involvement of Delta/Notch signaling in zebrafish adult pigment stripe patterning. Development 141:318–24
    [Google Scholar]
  39. 39. 
    Hawkes JW. 1974. The structure of fish skin. I. General organization. Cell Tissue Res 149:147–58
    [Google Scholar]
  40. 40. 
    Hirata M, Nakamura K, Kanemaru T, Shibata Y, Kondo S 2003. Pigment cell organization in the hypodermis of zebrafish. Dev. Dyn. 227:497–503
    [Google Scholar]
  41. 41. 
    Hirata M, Nakamura K, Kondo S 2005. Pigment cell distributions in different tissues of the zebrafish, with special reference to the striped pigment pattern. Dev. Dyn. 234:293–300
    [Google Scholar]
  42. 42. 
    Horstadius S. 1950. The Neural Crest: Its Properties and Derivatives in Light of Experimental Research London: Oxford Univ. Press
    [Google Scholar]
  43. 43. 
    Hou L, Pavan WJ. 2008. Transcriptional and signaling regulation in neural crest stem cell-derived melanocyte development: Do all roads lead to Mitf. ? Cell Res 18:1163–76
    [Google Scholar]
  44. 44. 
    Houde AE. 1997. Sex, Color, and Mate Choice in Guppies Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  45. 45. 
    Hubbard JK, Uy JA, Hauber ME, Hoekstra HE, Safran RJ 2010. Vertebrate pigmentation: from underlying genes to adaptive function. Trends Genet 26:231–39
    [Google Scholar]
  46. 46. 
    Hultman KA, Johnson SL. 2010. Differential contribution of direct-developing and stem cell-derived melanocytes to the zebrafish larval pigment pattern. Dev. Biol. 337:425–31
    [Google Scholar]
  47. 47. 
    Hutton P, Seymoure BM, McGraw KJ, Ligon RA, Simpson RK 2015. Dynamic color communication. Curr. Opin. Behav. Sci. 6:41–49
    [Google Scholar]
  48. 48. 
    Inaba M, Yamanaka H, Kondo S 2012. Pigment pattern formation by contact-dependent depolarization. Science 335:677
    [Google Scholar]
  49. 49. 
    Inoue S, Kondo S, Parichy DM, Watanabe M 2014. Tetraspanin 3c requirement for pigment cell interactions and boundary formation in zebrafish adult pigment stripes. Pigment Cell Melanoma Res 27:190–200
    [Google Scholar]
  50. 50. 
    Irion U, Frohnhöfer H-G, Krauss J, Çolak Champollion T, Maischein HM et al. 2014. Gap junctions composed of connexins 41.8 and 39.4 are essential for colour pattern formation in zebrafish. eLife 3:e05125
    [Google Scholar]
  51. 51. 
    Iwashita M, Watanabe M, Ishii M, Chen T, Johnson SL et al. 2006. Pigment pattern in jaguar/obelix zebrafish is caused by a Kir7.1 mutation: implications for the regulation of melanosome movement. PLOS Genet 2:e197
    [Google Scholar]
  52. 52. 
    Iyengar S, Kasheta M, Ceol CJ 2015. Poised regeneration of zebrafish melanocytes involves direct differentiation and concurrent replenishment of tissue-resident progenitor cells. Dev. Cell 33:631–43
    [Google Scholar]
  53. 53. 
    Johnson SL, Africa D, Walker C, Weston JA 1995. Genetic control of adult pigment stripe development in zebrafish. Dev. Biol. 167:27–33
    [Google Scholar]
  54. 54. 
    Johnson SL, Nguyen AN, Lister JA 2011. mitfa is required at multiple stages of melanocyte differentiation but not to establish the melanocyte stem cell. Dev. Biol. 350:405–13
    [Google Scholar]
  55. 55. 
    Kelsh RN, Sosa KC, Owen JP, Yates CA 2017. Zebrafish adult pigment stem cells are multipotent and form pigment cells by a progressive fate restriction process: Clonal analysis identifies shared origin of all pigment cell types. Bioessays 39:1600234
    [Google Scholar]
  56. 56. 
    Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF 1995. Stages of embryonic development of the zebrafish. Dev. Dyn. 203:253–310
    [Google Scholar]
  57. 57. 
    Kirschbaum F. 1975. Untersuchungen über das Farbmuster der Zebrabarbe Brachydanio rerio (Cyprinidae, Teleostei). Wilhelm Roux's Arch 177:129–52
    [Google Scholar]
  58. 58. 
    Kocher TD. 2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nat. Rev. Genet. 5:288–98
    [Google Scholar]
  59. 59. 
    Kottler VA, Fadeev A, Weigel D, Dreyer C 2013. Pigment pattern formation in the guppy, Poecilia reticulata, involves the Kita and Csf1ra receptor tyrosine kinases. Genetics 194:631–46
    [Google Scholar]
  60. 60. 
    Kottler VA, Koch I, Flotenmeyer M, Hashimoto H, Weigel D, Dreyer C 2014. Multiple pigment cell types contribute to the black, blue, and orange ornaments of male guppies (Poecilia reticulata). PLOS ONE 9:e85647
    [Google Scholar]
  61. 61. 
    Kratochwil CF, Liang Y, Gerwin J, Woltering JM, Urban S et al. 2018. Agouti-related peptide 2 facilitates convergent evolution of stripe patterns across cichlid fish radiations. Science 362:457–60
    [Google Scholar]
  62. 62. 
    Krauss J, Frohnhöfer H-G, Walderich B, Maischein HM, Weiler C et al. 2014. Endothelin signalling in iridophore development and stripe pattern formation of zebrafish. Biol. Open 3:503–9
    [Google Scholar]
  63. 63. 
    Kullander SO, Britz R. 2015. Description of Danio absconditus, new species, and redescription of Danio feegradei (Teleostei: Cyprinidae), from the Rakhine Yoma hotspot in south-western Myanmar. Zootaxa 3948:233–47
    [Google Scholar]
  64. 64. 
    Lang MR, Patterson LB, Gordon TN, Johnson SL, Parichy DM 2009. Basonuclin-2 requirements for zebrafish adult pigment pattern development and female fertility. PLOS Genet 5:e1000744
    [Google Scholar]
  65. 65. 
    Larson TA, Gordon TN, Lau HE, Parichy DM 2010. Defective adult oligodendrocyte and Schwann cell development, pigment pattern, and craniofacial morphology in puma mutant zebrafish having an alpha tubulin mutation. Dev. Biol. 346:296–309
    [Google Scholar]
  66. 66. 
    Le Douarin NM, Dupin E 2018. The “beginnings” of the neural crest. Dev. Biol. 444:Suppl. 1S3–13
    [Google Scholar]
  67. 67. 
    Le Guellec D, Morvan-Dubois G, Sire JY 2004. Skin development in bony fish with particular emphasis on collagen deposition in the dermis of the zebrafish (Danio rerio). Int. J. Dev. Biol. 48:217–31
    [Google Scholar]
  68. 68. 
    Lee H-O, Levorse JM, Shin MK 2003. The endothelin receptor-B is required for the migration of neural crest-derived melanocyte and enteric neuron precursors. Dev. Biol. 259:162–75
    [Google Scholar]
  69. 69. 
    Levy C, Khaled M, Fisher DE 2006. MITF: master regulator of melanocyte development and melanoma oncogene. Trends Mol. Med. 12:406–14
    [Google Scholar]
  70. 70. 
    Lewis VM, Saunders LM, Larson TA, Bain EJ, Sturiale SL et al. 2019. Fate plasticity and reprogramming in genetically distinct populations of Danio leucophores. PNAS 116:11806–11
    [Google Scholar]
  71. 71. 
    Lister JA, Close J, Raible DW 2001. Duplicate mitf genes in zebrafish: complementary expression and conservation of melanogenic potential. Dev. Biol. 237:333–44
    [Google Scholar]
  72. 72. 
    Lister JA, Robertson CP, Lepage T, Johnson SL, Raible DW 1999. nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126:3757–67
    [Google Scholar]
  73. 73. 
    Logan DW, Burn SF, Jackson IJ 2006. Regulation of pigmentation in zebrafish melanophores. Pigment Cell Res 19:206–13
    [Google Scholar]
  74. 74. 
    Lopes SS, Yang X, Müller J, Carney TJ, McAdow AR et al. 2008. Leukocyte tyrosine kinase functions in pigment cell development. PLOS Genet 4:e1000026
    [Google Scholar]
  75. 75. 
    Maderspacher F, Nüsslein-Volhard C. 2003. Formation of the adult pigment pattern in zebrafish requires leopard and obelix dependent cell interactions. Development 130:3447–57
    [Google Scholar]
  76. 76. 
    Mahabir S, Chatterjee D, Buske C, Gerlai R 2013. Maturation of shoaling in two zebrafish strains: a behavioral and neurochemical analysis. Behav. Brain Res. 247:1–8
    [Google Scholar]
  77. 77. 
    Mahalwar P, Singh AP, Fadeev A, Nüsslein-Volhard C, Irion U 2016. Heterotypic interactions regulate cell shape and density during color pattern formation in zebrafish. Biol. Open 5:1680–90
    [Google Scholar]
  78. 78. 
    Mahalwar P, Walderich B, Singh AP, Nüsslein-Volhard C 2014. Local reorganization of xanthophores fine-tunes and colors the striped pattern of zebrafish. Science 345:1362–64
    [Google Scholar]
  79. 79. 
    Manukyan L, Montandon SA, Fofonjka A, Smirnov S, Milinkovitch MC 2017. A living mesoscopic cellular automaton made of skin scales. Nature 544:173–79
    [Google Scholar]
  80. 80. 
    Marshall NJ, Cortesi F, de Busserolles F, Siebeck UE, Cheney KL 2018. Colours and colour vision in reef fishes: past, present and future research directions. J. Fish Biol. https://doi.org/10.1111/jfb.13849
    [Crossref] [Google Scholar]
  81. 81. 
    McCann LI, Carlson CC. 1982. Effect of cross-rearing on species identification in zebra fish and pearl danios. Dev. Psychobiol. 15:71–74
    [Google Scholar]
  82. 82. 
    McClure M. 1999. Development and evolution of melanophore patterns in fishes of the genus Danio (Teleostei: Cyprinidae). J. Morphol. 241:83–105
    [Google Scholar]
  83. 83. 
    McCluskey BM, Postlethwait JH. 2015. Phylogeny of zebrafish, a “model species,” within Danio, a “model genus. .” Mol. Biol. Evol. 32:635–52
    [Google Scholar]
  84. 84. 
    McMenamin SK, Bain EJ, McCann AE, Patterson LB, Eom DS et al. 2014. Thyroid hormone-dependent adult pigment cell lineage and pattern in zebrafish. Science 345:1358–61
    [Google Scholar]
  85. 85. 
    McMenamin SK, Chandless MN, Parichy DM 2016. Working with zebrafish at postembryonic stages. Methods Cell Biol 134:587–607
    [Google Scholar]
  86. 86. 
    McMenamin SK, Parichy DM. 2013. Metamorphosis in teleosts. Curr. Top. Dev. Biol. 103:127–65
    [Google Scholar]
  87. 87. 
    Miller CT, Beleza S, Pollen AA, Schluter D, Kittles RA et al. 2007. cis-Regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131:1179–89
    [Google Scholar]
  88. 88. 
    Mills MG, Nuckels RJ, Parichy DM 2007. Deconstructing evolution of adult phenotypes: genetic analyses of kit reveal homology and evolutionary novelty during adult pigment pattern development of Danio fishes. Development 134:1081–90
    [Google Scholar]
  89. 89. 
    Milos N, Dingle AD. 1978. Dynamics of pigment pattern formation in the zebrafish, Brachydanio rerio. I. Establishment and regulation of the lateral line melanophore stripe during the first eight days of development. J. Exp. Zool. 205:205–16
    [Google Scholar]
  90. 90. 
    Milos N, Dingle AD. 1978. Dynamics of pigment pattern formation in the zebrafish, Brachydanio rerio. II. Lability of lateral line stripe formation and regulation of pattern defects. J. Exp. Zool. 205:217–24
    [Google Scholar]
  91. 91. 
    Milos N, Dingle AD, Milos JP 1983. Dynamics of pigment pattern formation in the zebrafish, Brachydanio rerio. III. Effect of anteroposterior location of three-day lateral line melanophores on colonization by the second wave of melanophores. J. Exp. Zool. 227:81–92
    [Google Scholar]
  92. 92. 
    Minchin JE, Hughes SM. 2008. Sequential actions of Pax3 and Pax7 drive xanthophore development in zebrafish neural crest. Dev. Biol. 317:508–22
    [Google Scholar]
  93. 93. 
    Mo ES, Cheng Q, Reshetnyak AV, Schlessinger J, Nicoli S 2017. Alk and Ltk ligands are essential for iridophore development in zebrafish mediated by the receptor tyrosine kinase Ltk. PNAS 114:12027–32
    [Google Scholar]
  94. 94. 
    Mort RL, Jackson IJ, Patton EE 2015. The melanocyte lineage in development and disease. Development 142:620–32
    [Google Scholar]
  95. 95. 
    Murakami A, Hasegawa M, Kuriyama T 2016. Pigment cell mechanism of postembryonic stripe pattern formation in the Japanese four-lined snake. J. Morphol. 277:196–203
    [Google Scholar]
  96. 96. 
    Nagao Y, Suzuki T, Shimizu A, Kimura T, Seki R et al. 2014. Sox5 functions as a fate switch in medaka pigment cell development. PLOS Genet 10:e1004246
    [Google Scholar]
  97. 97. 
    Nagao Y, Takada H, Miyadai M, Adachi T, Seki R et al. 2018. Distinct interactions of Sox5 and Sox10 in fate specification of pigment cells in medaka and zebrafish. PLOS Genet 14:e1007260
    [Google Scholar]
  98. 98. 
    Nakamasu A, Takahashi G, Kanbe A, Kondo S 2009. Interactions between zebrafish pigment cells responsible for the generation of Turing patterns. PNAS 106:8429–34
    [Google Scholar]
  99. 99. 
    Nguyen PD, Hollway GE, Sonntag C, Miles LB, Hall TE et al. 2014. Haematopoietic stem cell induction by somite-derived endothelial cells controlled by meox1. Nature 512:314–18
    [Google Scholar]
  100. 100. 
    Nord H, Dennhag N, Muck J, von Hofsten J 2016. Pax7 is required for establishment of the xanthophore lineage in zebrafish embryos. Mol. Biol. Cell 27:1853–62
    [Google Scholar]
  101. 101. 
    Opdecamp K, Nakayama A, Nguyen MT, Hodgkinson CA, Pavan WJ, Arnheiter H 1997. Melanocyte development in vivo and in neural crest cell cultures: crucial dependence on the Mitf basic-helix-loop-helix-zipper transcription factor. Development 124:2377–86
    [Google Scholar]
  102. 102. 
    O'Reilly-Pol T, Johnson SL. 2008. Neocuproine ablates melanocytes in adult zebrafish. Zebrafish 5:257–64
    [Google Scholar]
  103. 103. 
    Oshima N, Kasai A. 2002. Iridophores involved in generation of skin color in the zebrafish, Brachydanio rerio. Forma 17:91–101
    [Google Scholar]
  104. 104. 
    Parichy DM. 1996. Pigment patterns of larval salamanders (Ambystomatidae, Salamandridae): the role of the lateral line sensory system and the evolution of pattern-forming mechanisms. Dev. Biol. 175:265–82
    [Google Scholar]
  105. 105. 
    Parichy DM, Elizondo MR, Mills MG, Gordon TN, Engeszer RE 2009. Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish. Dev. Dyn. 238:2975–3015
    [Google Scholar]
  106. 106. 
    Parichy DM, Johnson SL. 2001. Zebrafish hybrids suggest genetic mechanisms for pigment pattern diversification in Danio. Dev. Genes Evol 211:319–28
    [Google Scholar]
  107. 107. 
    Parichy DM, Mellgren EM, Rawls JF, Lopes SS, Kelsh RN, Johnson SL 2000. Mutational analysis of endothelin receptor b1 (rose) during neural crest and pigment pattern development in the zebrafish Danio rerio.. Dev. Biol 227:294–306
    [Google Scholar]
  108. 108. 
    Parichy DM, Ransom DG, Paw B, Zon LI, Johnson SL 2000. An orthologue of the kit-related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio. Development 127:3031–44
    [Google Scholar]
  109. 109. 
    Parichy DM, Rawls JF, Pratt SJ, Whitfield TT, Johnson SL 1999. Zebrafish sparse corresponds to an orthologue of c-kit and is required for the morphogenesis of a subpopulation of melanocytes, but is not essential for hematopoiesis or primordial germ cell development. Development 126:3425–36
    [Google Scholar]
  110. 110. 
    Parichy DM, Turner JM. 2003. Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development. Development 130:817–33
    [Google Scholar]
  111. 111. 
    Parichy DM, Turner JM. 2003. Zebrafish puma mutant decouples pigment pattern and somatic metamorphosis. Dev. Biol. 256:242–57
    [Google Scholar]
  112. 112. 
    Parichy DM, Turner JM, Parker NB 2003. Essential role for puma in development of postembryonic neural crest-derived cell lineages in zebrafish. Dev. Biol. 256:221–41
    [Google Scholar]
  113. 113. 
    Patterson LB, Bain EJ, Parichy DM 2014. Pigment cell interactions and differential xanthophore recruitment underlying zebrafish stripe reiteration and Danio pattern evolution. Nat. Commun. 5:5299
    [Google Scholar]
  114. 114. 
    Patterson LB, Parichy DM. 2013. Interactions with iridophores and the tissue environment required for patterning melanophores and xanthophores during zebrafish adult pigment stripe formation. PLOS Genet 9:e1003561
    [Google Scholar]
  115. 115. 
    Pavan WJ, Tilghman SM. 1994. Piebald lethal (sl) acts early to disrupt the development of neural crest-derived melanocytes. PNAS 91:7159–63
    [Google Scholar]
  116. 116. 
    Petratou K, Subkhankulova T, Lister JA, Rocco A, Schwetlick H, Kelsh RN 2018. A systems biology approach uncovers the core gene regulatory network governing iridophore fate choice from the neural crest. PLOS Genet 14:e1007402
    [Google Scholar]
  117. 117. 
    Pierre-Jerome E, Jang SS, Havens KA, Nemhauser JL, Klavins E 2014. Recapitulation of the forward nuclear auxin response pathway in yeast. PNAS 111:9407–12
    [Google Scholar]
  118. 118. 
    Price AC, Weadick CJ, Shim J, Rodd FH 2008. Pigments, patterns, and fish behavior. Zebrafish 5:297–307
    [Google Scholar]
  119. 119. 
    Quigley IK, Manuel JL, Roberts RA, Nuckels RJ, Herrington ER et al. 2005. Evolutionary diversification of pigment pattern in Danio fishes: differential fms dependence and stripe loss in D. albolineatus. Development 132:89–104
    [Google Scholar]
  120. 120. 
    Quigley IK, Turner JM, Nuckels RJ, Manuel JL, Budi EH et al. 2004. Pigment pattern evolution by differential deployment of neural crest and post-embryonic melanophore lineages in Danio fishes. Development 131:6053–69
    [Google Scholar]
  121. 121. 
    Rawls JF, Johnson SL. 2003. Temporal and molecular separation of the kit receptor tyrosine kinase's roles in zebrafish melanocyte migration and survival. Dev. Biol. 262:152–61
    [Google Scholar]
  122. 122. 
    Roberts RB, Ser JR, Kocher TD 2009. Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science 326:998–1001
    [Google Scholar]
  123. 123. 
    Rosenthal GG, Ryan MJ. 2005. Assortative preferences for stripes in danios. Anim. Behav. 70:1063–66
    [Google Scholar]
  124. 124. 
    Russell ES. 1949. Analysis of pleiotropism at the W-locus in the mouse: relationship between the effects of W and Wv substitution on hair pigmentation and erythrocytes. Genetics 34:708–23
    [Google Scholar]
  125. 125. 
    Salis P, Lorin T, Lewis V, Rey C, Marcionetti A et al. 2019. Developmental and comparative transcriptomic identification of iridophore contribution to white barring in clownfish. Pigment Cell Melanoma Res 32:391–402
    [Google Scholar]
  126. 126. 
    Salis P, Roux N, Soulat O, Lecchini D, Laudet V, Frédérich B 2018. Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes. BMC Biol 16:90
    [Google Scholar]
  127. 127. 
    Salzburger W. 2009. The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol. Ecol. 18:169–85
    [Google Scholar]
  128. 128. 
    Salzburger W, Braasch I, Meyer A 2007. Adaptive sequence evolution in a color gene involved in the formation of the characteristic egg-dummies of male haplochromine cichlid fishes. BMC Biol 5:51
    [Google Scholar]
  129. 129. 
    Santos ME, Braasch I, Boileau N, Meyer BS, Sauteur L et al. 2014. The evolution of cichlid fish egg-spots is linked with a cis-regulatory change. Nat. Commun. 5:5149
    [Google Scholar]
  130. 130. 
    Saunders LM, Mishra AK, Aman AJ, Lewis VM, Toomey MB et al. 2019. Thyroid hormone regulates distinct paths to maturation in pigment cell lineages. eLife 8:e45181
    [Google Scholar]
  131. 131. 
    Sawada R, Aramaki T, Kondo S 2018. Flexibility of pigment cell behavior permits the robustness of skin pattern formation. Genes Cells 23:537–45
    [Google Scholar]
  132. 132. 
    Schneider RA. 2018. Neural crest and the origin of species-specific pattern. Genesis 56:e23219
    [Google Scholar]
  133. 133. 
    Singh AP, Dinwiddie A, Mahalwar P, Schach U, Linker C et al. 2016. Pigment cell progenitors in zebrafish remain multipotent through metamorphosis. Dev. Cell 38:316–30
    [Google Scholar]
  134. 134. 
    Singh AP, Frohnhöfer H-G, Irion U, Nüsslein-Volhard C 2015. Response to comment on “Local reorganization of xanthophores fine-tunes and colors the striped pattern of zebrafish. .” Science 348:297
    [Google Scholar]
  135. 135. 
    Singh AP, Schach U, Nüsslein-Volhard C 2014. Proliferation, dispersal and patterned aggregation of iridophores in the skin prefigure striped colouration of zebrafish. Nat. Cell Biol. 16:607–14
    [Google Scholar]
  136. 136. 
    Spiewak JE, Bain EJ, Liu J, Kou K, Sturiale SL et al. 2018. Evolution of Endothelin signaling and diversification of adult pigment pattern in Danio fishes. PLOS Genet 14:e1007538
    [Google Scholar]
  137. 137. 
    Streisinger G, Singer F, Walker C, Knauber D, Dower N 1986. Segregation analyses and gene-centromere distances in zebrafish. Genetics 112:311–19
    [Google Scholar]
  138. 138. 
    Sugimoto M, Yuki M, Miyakoshi T, Maruko K 2005. The influence of long-term chromatic adaptation on pigment cells and striped pigment patterns in the skin of the zebrafish, Danio rerio. J. Exp. Zool. 303:430–40
    [Google Scholar]
  139. 139. 
    Svetic V, Hollway GE, Elworthy S, Chipperfield TR, Davison C et al. 2007. Sdf1a patterns zebrafish melanophores and links the somite and melanophore pattern defects in choker mutants. Development 134:1011–22
    [Google Scholar]
  140. 140. 
    Szabó A, Mayor R. 2018. Mechanisms of neural crest migration. Annu. Rev. Genet. 52:43–63
    [Google Scholar]
  141. 141. 
    Takahashi G, Kondo S. 2008. Melanophores in the stripes of adult zebrafish do not have the nature to gather, but disperse when they have the space to move. Pigment Cell Melanoma Res 21:677–86
    [Google Scholar]
  142. 142. 
    Twitty VC, Bodenstein D. 1939. Correlated genetic and embryological experiments on Triturus. J. Exp. Zool 81:357–98
    [Google Scholar]
  143. 143. 
    Vibert L, Aquino G, Gehring I, Subkankulova T, Schilling TF et al. 2017. An ongoing role for Wnt signaling in differentiating melanocytes in vivo. Pigment Cell Melanoma Res 30:219–32
    [Google Scholar]
  144. 144. 
    Volkening A, Sandstede B. 2015. Modelling stripe formation in zebrafish: an agent-based approach. J. R. Soc. Interface 12:20150812
    [Google Scholar]
  145. 145. 
    Walderich B, Singh AP, Mahalwar P, Nüsslein-Volhard C 2016. Homotypic cell competition regulates proliferation and tiling of zebrafish pigment cells during colour pattern formation. Nat. Commun. 7:11462
    [Google Scholar]
  146. 146. 
    Watanabe M, Iwashita M, Ishii M, Kurachi Y, Kawakami A et al. 2006. Spot pattern of leopard Danio is caused by mutation in the zebrafish connexin41.8 gene. EMBO Rep 7:893–97
    [Google Scholar]
  147. 147. 
    Watanabe M, Kondo S. 2012. Changing clothes easily: connexin41.8 regulates skin pattern variation. Pigment Cell Melanoma Res 25:326–30
    [Google Scholar]
  148. 148. 
    Watanabe M, Kondo S. 2015. Comment on “Local reorganization of xanthophores fine-tunes and colors the striped pattern of zebrafish. .” Science 348:297
    [Google Scholar]
  149. 149. 
    Watanabe M, Kondo S. 2015. Is pigment patterning in fish skin determined by the Turing mechanism?. Trends Genet 31:88–96
    [Google Scholar]
  150. 150. 
    Watanabe M, Sawada R, Aramaki T, Skerrett IM, Kondo S 2016. The physiological characterization of Connexin41.8 and Connexin39.4, which are involved in the striped pattern formation of zebrafish. J. Biol. Chem. 291:1053–63
    [Google Scholar]
  151. 151. 
    Watanabe M, Watanabe D, Kondo S 2012. Polyamine sensitivity of gap junctions is required for skin pattern formation in zebrafish. Sci. Rep. 2:473
    [Google Scholar]
  152. 152. 
    Windner SE, Bird NC, Patterson SE, Doris RA, Devoto SH 2012. Fss/Tbx6 is required for central dermomyotome cell fate in zebrafish. Biol. Open 1:806–14
    [Google Scholar]
  153. 153. 
    Woodcock MR, Vaughn-Wolfe J, Elias A, Kump DK, Kendall KD et al. 2017. Identification of mutant genes and introgressed tiger salamander DNA in the laboratory axolotl, Ambystoma mexicanum. Sci. Rep. 7:6
    [Google Scholar]
  154. 154. 
    Yamaguchi M, Yoshimoto E, Kondo S 2007. Pattern regulation in the stripe of zebrafish suggests an underlying dynamic and autonomous mechanism. PNAS 104:4790–93
    [Google Scholar]
  155. 155. 
    Yamanaka H, Kondo S. 2014. In vitro analysis suggests that difference in cell movement during direct interaction can generate various pigment patterns in vivo. PNAS 111:1867–72
    [Google Scholar]
  156. 156. 
    Zeng Z, Johnson SL, Lister JA, Patton EE 2015. Temperature-sensitive splicing of mitfa by an intron mutation in zebrafish. Pigment Cell Melanoma Res 28:229–32
    [Google Scholar]
  157. 157. 
    Zhang YM, Zimmer MA, Guardia T, Callahan SJ, Mondal C et al. 2018. Distant insulin signaling regulates vertebrate pigmentation through the Sheddase Bace2. Dev. Cell 45:580–94.e7
    [Google Scholar]
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