Abstract
Teleosts comprise roughly half of all vertebrates and exhibit a diverse array of pigment cells and pigment patterns that function in behaviors ranging from camouflage to mate choice. This chapter examines recent advances in understanding the developmental genetics of teleost pigment cells and pattern formation, and how comparative studies across species and populations are providing insights into fundamental aspects of vertebrate development and evolution.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alberch P, Gould SJ, Oster GF, Wake DB (1979) Size and shape in ontogeny and phylogeny. Paleobiology 5:296–317
Baldwin CC (2013) The phylogenetic significance of colour patterns in marine teleost larvae. Zool J Linnean Soc 168(3):496–563. https://doi.org/10.1111/zoj.12033
Besmer P, Manova K, Duttlinger R, Huang EJ, Packer A, Gyssler C, Bachvarova RF (1993) The kit-ligand (steel factor) and its receptor c-kit/W: pleiotropic roles in gametogenesis and melanogenesis. Dev Suppl 1993:125–137
Braasch I (2006) Asymmetric evolution in two fish-specifically duplicated receptor tyrosine kinase paralogons involved in teleost coloration. Mol Biol Evol 23(6):1192–1202. https://doi.org/10.1093/molbev/msk003
Braasch I, Postlethwait JH (2011) The teleost agouti-related protein 2 gene is an ohnolog gone missing from the tetrapod genome. Proc Natl Acad Sci U S A 108(13):E47–E48. https://doi.org/10.1073/pnas.1101594108
Braasch I, Schartl M (2014) Evolution of endothelin receptors in vertebrates. Gen Comp Endocrinol 209:21–34. https://doi.org/10.1016/j.ygcen.2014.06.028
Braasch I, Salzburger W, Meyer A (2006) Asymmetric evolution in two fish-specifically duplicated receptor tyrosine kinase paralogons involved in teleost coloration. Mol Biol Evol 23(6):1192–1202. https://doi.org/10.1093/molbev/msk003
Braasch I, Schartl M, Volff JN (2007) Evolution of pigment synthesis pathways by gene and genome duplication in fish. BMC Evol Biol 7:74. https://doi.org/10.1186/1471-2148-7-74
Braasch I, Volff JN, Schartl M (2008) The evolution of teleost pigmentation and the fish-specific genome duplication. J Fish Biol 73(8):1891–1918. https://doi.org/10.1111/j.1095-8649.2008.02011.x
Braasch I, Brunet F, Volff JN, Schartl M (2009a) Pigmentation pathway evolution after whole-genome duplication in fish. Genome Biol Evol 1:479–493. https://doi.org/10.1093/gbe/evp050
Braasch I, Liedtke D, Volff JN, Schartl M (2009b) Pigmentary function and evolution of tyrp1 gene duplicates in fish. Pigment Cell Melanoma Res 22(6):839–850. https://doi.org/10.1111/j.1755-148X.2009.00614.x
Braasch I, Volff JN, Schartl M (2009c) The endothelin system: evolution of vertebrate-specific ligand-receptor interactions by three rounds of genome duplication. Mol Biol Evol 26(4):783–799
Braasch I, Peterson SM, Desvignes T, McCluskey BM, Batzel P, Postlethwait JH (2015) A new model army: emerging fish models to study the genomics of vertebrate evo-devo. J Exp Zool B Mol Dev Evol 324(4):316–341. https://doi.org/10.1002/jez.b.22589
Braasch I, Gehrke AR, Smith JJ, Kawasaki K, Manousaki T, Pasquier J, Amores A, Desvignes T, Batzel P, Catchen J, Berlin AM, Campbell MS, Barrell D, Martin KJ, Mulley JF, Ravi V, Lee AP, Nakamura T, Chalopin D, Fan S, Wcisel D, Canestro C, Sydes J, Beaudry FE, Sun Y, Hertel J, Beam MJ, Fasold M, Ishiyama M, Johnson J, Kehr S, Lara M, Letaw JH, Litman GW, Litman RT, Mikami M, Ota T, Saha NR, Williams L, Stadler PF, Wang H, Taylor JS, Fontenot Q, Ferrara A, Searle SM, Aken B, Yandell M, Schneider I, Yoder JA, Volff JN, Meyer A, Amemiya CT, Venkatesh B, Holland PW, Guiguen Y, Bobe J, Shubin NH, Di Palma F, Alfoldi J, Lindblad-Toh K, Postlethwait JH (2016) The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. Nat Genet 48(4):427–437. https://doi.org/10.1038/ng.3526
Brawand D, Wagner CE, Li YI, Malinsky M, Keller I, Fan S, Simakov O, Ng AY, Lim ZW, Bezault E, Turner-Maier J, Johnson J, Alcazar R, Noh HJ, Russell P, Aken B, Alfoldi J, Amemiya C, Azzouzi N, Baroiller JF, Barloy-Hubler F, Berlin A, Bloomquist R, Carleton KL, Conte MA, D'Cotta H, Eshel O, Gaffney L, Galibert F, Gante HF, Gnerre S, Greuter L, Guyon R, Haddad NS, Haerty W, Harris RM, Hofmann HA, Hourlier T, Hulata G, Jaffe DB, Lara M, Lee AP, MacCallum I, Mwaiko S, Nikaido M, Nishihara H, Ozouf-Costaz C, Penman DJ, Przybylski D, Rakotomanga M, Renn SC, Ribeiro FJ, Ron M, Salzburger W, Sanchez-Pulido L, Santos ME, Searle S, Sharpe T, Swofford R, Tan FJ, Williams L, Young S, Yin S, Okada N, Kocher TD, Miska EA, Lander ES, Venkatesh B, Fernald RD, Meyer A, Ponting CP, Streelman JT, Lindblad-Toh K, Seehausen O, Di Palma F (2014) The genomic substrate for adaptive radiation in African cichlid fish. Nature 513(7518):375–381. https://doi.org/10.1038/nature13726
Budd PL (1940) Development of the eggs and early larvae of six california fishes. Hopkins Marine Station Stanford University, fish bulletin No. 56
Budi EH, Patterson LB, Parichy DM (2008) Embryonic requirements for ErbB signaling in neural crest development and adult pigment pattern formation. Development 135(15):2603–2614. https://doi.org/10.1242/dev.019299
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(5):e1002044. https://doi.org/10.1371/journal.pgen.1002044
Bullara D, De Decker Y (2015) Pigment cell movement is not required for generation of Turing patterns in zebrafish skin. Nat Commun 6:7971. https://doi.org/10.1038/ncomms7971
Caicedo-Carvajal CE, Shinbrot T (2008) In silico zebrafish pattern formation. Dev Biol 315(2):397–403. https://doi.org/10.1016/j.ydbio.2007.12.036
Cal L, MegIas M, Cerda-Reverter JM, Postlethwait JH, Braasch I, Rotllant J (2017a) BAC recombineering of the agouti loci from spotted gar and zebrafish reveals the evolutionary ancestry of dorsal-ventral pigment asymmetry in fish. J Exp Zool B Mol Dev Evol 328(7):697–708. https://doi.org/10.1002/jez.b.22748
Cal L, Suarez-Bregua P, Cerda-Reverter JM, Braasch I, Rotllant J (2017b) Fish pigmentation and the melanocortin system. Comp Biochem Physiol A Mol Integr Physiol 211:26–33. https://doi.org/10.1016/j.cbpa.2017.06.001
Cal L, Suarez-Bregua P, Comesana P, Owen J, Braasch I, Kelsh R, Cerda-Reverter JM, Rotllant J (2019) Countershading in zebrafish results from an Asip1 controlled dorsoventral gradient of pigment cell differentiation. Sci Rep 9(1):3449. https://doi.org/10.1038/s41598-019-40251-z
Camargo Sosa K, Colanesi S, Muller J, Schulte-Merker S, Stemple D, Patton EE, Kelsh RN (2019) Endothelin receptor Aa regulates proliferation and differentiation of Erb-dependant pigment progenitors in zebrafish. PLoS Genet. https://doi.org/10.1101/308221
Ceinos RM, Guillot R, Kelsh RN, Cerda-Reverter JM, Rotllant J (2015) Pigment patterns in adult fish result from superimposition of two largely independent pigmentation mechanisms. Pigment Cell Melanoma Res 28(2):196–209. https://doi.org/10.1111/pcmr.12335
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(3):1597–1610. https://doi.org/10.1210/en.2004-1346
Crawford NG, Kelly DE, Hansen MEB, Beltrame MH, Fan S, Bowman SL, Jewett E, Ranciaro A, Thompson S, Lo Y, Pfeifer SP, Jensen JD, Campbell MC, Beggs W, Hormozdiari F, Mpoloka SW, Mokone GG, Nyambo T, Meskel DW, Belay G, Haut J, Program NCS, Rothschild H, Zon L, Zhou Y, Kovacs MA, Xu M, Zhang T, Bishop K, Sinclair J, Rivas C, Elliot E, Choi J, Li SA, Hicks B, Burgess S, Abnet C, Watkins-Chow DE, Oceana E, Song YS, Eskin E, Brown KM, Marks MS, Loftus SK, Pavan WJ, Yeager M, Chanock S, Tishkoff SA (2017) Loci associated with skin pigmentation identified in African populations. Science 358(6365). https://doi.org/10.1126/science.aan8433
Cronk QC (2009) Evolution in reverse gear: the molecular basis of loss and reversal. Cold Spring Harb Symp Quant Biol 74:259–266. https://doi.org/10.1101/sqb.2009.74.034
Curran K, Raible DW, Lister JA (2009) Foxd3 controls melanophore specification in the zebrafish neural crest by regulation of Mitf. Dev Biol 332(2):408–417
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 344:107–118
Davis AL, Thomas KN, Goetz FE, Robison BH, Johnsen S, Osborn KJ (2020) Ultra-black camouflage in deep-sea fishes. Curr Biol 30(17):3470–3476. https://doi.org/10.1016/j.cub.2020.06.044
Dehal P, Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3(10):e314. https://doi.org/10.1371/journal.pbio.0030314
Dooley CM, Mongera A, Walderich B, Nusslein-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(5):1003–1013. https://doi.org/10.1242/dev.087007
Dupin E, Calloni GW, Coelho-Aguiar JM, Le Douarin NM (2018) The issue of the multipotency of the neural crest cells. Dev Biol 444(Suppl 1):S47–S59. https://doi.org/10.1016/j.ydbio.2018.03.024
Dushane GP (1934) The origin of pigment cells in Amphibia. Science 80(2087):620–621. https://doi.org/10.1126/science.80.2087.620-a
Dutton KA, Pauliny A, Lopes SS, Elworthy S, Carney TJ, Rauch J, Geisler R, Haffter P, Kelsh RN (2001) Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 128(21):4113–4125
Elworthy S, Lister JA, Carney TJ, Raible DW, Kelsh RN (2003) Transcriptional regulation of mitfa accounts for the sox10 requirement in zebrafish melanophore development. Development 130(12):2809–2818. https://doi.org/10.1242/dev.00461
Endler JA (1978) A predator’s view of animal color patterns. In: Hecht MK, Steere WC, Wallace B (eds) Evolutionary biology. Springer, Boston, MA, pp 319–364. https://doi.org/10.1007/978-1-4615-6956-5_5
Endler JA (1983) Natural and sexual selection on color patterns in Poeciliid fishes. Environ Biol Fishes 9:173–190
Eom DS, Parichy DM (2017) A macrophage relay for long-distance signaling during postembryonic tissue remodeling. Science 355(6331):1317–1320. https://doi.org/10.1126/science.aal2745
Eom DS, Inoue S, Patterson LB, Gordon TN, Slingwine R, Kondo S, Watanabe M, Parichy DM (2012) Melanophore migration and survival during zebrafish adult pigment stripe development require the immunoglobulin superfamily adhesion molecule Igsf11. PLoS Genet 8(8):e1002899. https://doi.org/10.1371/journal.pgen.1002899
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. https://doi.org/10.7554/eLife.12401
Eskova A, Frohnhofer HG, Nusslein-Volhard C, Irion U (2020) Galanin signaling in the brain regulates color pattern formation in zebrafish. Curr Biol 30(2):298–303. https://doi.org/10.1016/j.cub.2019.11.033
Espinasa L, Robinson J, Espinasa M (2018) Mc1r gene in Astroblepus pholeter and Astyanax mexicanus: convergent regressive evolution of pigmentation across cavefish species. Dev Biol 441(2):305–310. https://doi.org/10.1016/j.ydbio.2018.07.016
Fadeev A, Krauss J, Frohnhofer HG, Irion U, Nusslein-Volhard C (2015) Tight junction protein 1a regulates pigment cell organisation during zebrafish colour patterning. elife 4:e06545. https://doi.org/10.7554/eLife.06545
Fadeev A, Krauss J, Singh AP, Nusslein-Volhard C (2016) Zebrafish Leucocyte tyrosine kinase controls iridophore establishment, proliferation and survival. Pigment Cell Melanoma Res 29(3):284–296. https://doi.org/10.1111/pcmr.12454
Fadeev A, Mendoza-Garcia P, Irion U, Guan J, Pfeifer K, Wiessner S, Serluca F, Singh AP, Nusslein-Volhard C, Palmer RH (2018) ALKALs are in vivo ligands for ALK family receptor tyrosine kinases in the neural crest and derived cells. Proc Natl Acad Sci U S A 115(4):E630–E638. https://doi.org/10.1073/pnas.1719137115
Fitch KR, McGowan KA, van Raamsdonk CD, Fuchs H, Lee D, Puech A, Herault Y, Threadgill DW, Hrabe de Angelis M, Barsh GS (2003) Genetics of dark skin in mice. Genes Dev 17(2):214–228
Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151(4):1531–1545
Frohnhofer HG, Krauss J, Maischein HM, Nusslein-Volhard C (2013) Iridophores and their interactions with other chromatophores are required for stripe formation in zebrafish. Development 140(14):2997–3007. https://doi.org/10.1242/dev.096719
Fujii R (1993) Cytophysiology of fish chromatophores. Int Rev Cytol 143:191–255
Fukamachi S, Asakawa S, Wakamatsu Y, Shimizu N, Mitani H, Shima A (2004) Conserved function of medaka pink-eyed dilution in melanin synthesis and its divergent transcriptional regulation in gonads among vertebrates. Genetics 168(3):1519–1527. https://doi.org/10.1534/genetics.104.030494
Fukuzawa T (2010) Unusual development of light-reflecting pigment cells in intact and regenerating tail in the periodic albino mutant of Xenopus laevis. Cell Tissue Res 342(1):53–66. https://doi.org/10.1007/s00441-010-1042-0
Gould SJ (1977) Ontogeny and phylogeny. Harvard University Press, Cambridge, MA
Granneman JG, Kimler VA, Zhang H, Ye X, Luo X, Postlethwait JH, Thummel R (2017) Lipid droplet biology and evolution illuminated by the characterization of a novel perilipin in teleost fish. elife 6:21771. https://doi.org/10.7554/eLife.21771
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(9):e1002265. https://doi.org/10.1371/journal.pgen.1002265
Gross JB, Wilkens H (2013) Albinism in phylogenetically and geographically distinct populations of Astyanax cavefish arises through the same loss-of-function Oca2 allele. Heredity 111(2):122–130. https://doi.org/10.1038/hdy.2013.26
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(1):e1000326. https://doi.org/10.1371/journal.pgen.1000326
Gross JB, Weagley J, Stahl BA, Ma L, Espinasa L, McGaugh SE (2018) A local duplication of the Melanocortin receptor 1 locus in Astyanax. Genome 61(4):254–265. https://doi.org/10.1139/gen-2017-0049
Guillot R, Ceinos RM, Cal R, Rotllant J, Cerda-Reverter JM (2012) Transient ectopic overexpression of agouti-signalling protein 1 (asip1) induces pigment anomalies in flatfish. PLoS One 7(12):e48526. https://doi.org/10.1371/journal.pone.0048526
Gur D, Palmer BA, Weiner S, Addadi L (2016) Light manipulation by guanine crystals in organisms: biogenic scatterers, mirrors, multilayer reflectors and photonic crystals. Adv Funct Mater 2016:1603514
Gur D, Bain E, Johnson K, Aman AJ, Pasoili A, Flynn JD, Allen MC, Deheyn DD, Lee JC, Lippincott-Schwartz J, Parichy D (2020) In situ differentiation of iridophore crystallotypes underlies zebrafish stripe patterning. Nat Commun 11:6391
Hall BK (2003) Descent with modification: the unity underlying homology and homoplasy as seen through an analysis of development and evolution. Biol Rev 78(3):409–433. https://doi.org/10.1017/S1464793102006097
Hama T (1975) Chromatophores and iridocytes. In: Yamamoto T (ed) Medaka (killifish) biology and strains. Keigaku Publishing Co., Tokyo, pp 138–153
Hamada H, Watanabe M, Lau HE, Nishida T, Hasegawa T, Parichy DM, Kondo S (2014) Involvement of delta/notch signaling in zebrafish adult pigment stripe patterning. Development 141(2):318–324. https://doi.org/10.1242/dev.099804
Hemingson CR, Cowman PF, Hodge JR, Bellwood DR (2019) Colour pattern divergence in reef fish species is rapid and driven by both range overlap and symmetry. Ecol Lett 22(1):190–199. https://doi.org/10.1111/ele.13180
Hendrick LA, Carter GA, Hilbrands EH, Heubel BP, Schilling TF, Le Pabic P (2019) Bar, stripe and spot development in sand-dwelling cichlids from Lake Malawi. EvoDevo 10:18. https://doi.org/10.1186/s13227-019-0132-7
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(5783):101–104
Holzer G, Besson M, Lambert A, Francois L, Barth P, Gillet B, Hughes S, Piganeau G, Leulier F, Viriot L, Lecchini D, Laudet V (2017) Fish larval recruitment to reefs is a thyroid hormone-mediated metamorphosis sensitive to the pesticide chlorpyrifos. elife 6:e27595. https://doi.org/10.7554/eLife.27595
Hörstadius S (1950) The neural crest: its properties and derivatives in light of experimental research. Oxford University Press, London
Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, Princeton
Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, McLaren S, Sealy I, Caccamo M, Churcher C, Scott C, Barrett JC, Koch R, Rauch GJ, White S, Chow W, Kilian B, Quintais LT, Guerra-Assuncao JA, Zhou Y, Gu Y, Yen J, Vogel JH, Eyre T, Redmond S, Banerjee R, Chi J, Fu B, Langley E, Maguire SF, Laird GK, Lloyd D, Kenyon E, Donaldson S, Sehra H, Almeida-King J, Loveland J, Trevanion S, Jones M, Quail M, Willey D, Hunt A, Burton J, Sims S, McLay K, Plumb B, Davis J, Clee C, Oliver K, Clark R, Riddle C, Elliot D, Threadgold G, Harden G, Ware D, Begum S, Mortimore B, Kerry G, Heath P, Phillimore B, Tracey A, Corby N, Dunn M, Johnson C, Wood J, Clark S, Pelan S, Griffiths G, Smith M, Glithero R, Howden P, Barker N, Lloyd C, Stevens C, Harley J, Holt K, Panagiotidis G, Lovell J, Beasley H, Henderson C, Gordon D, Auger K, Wright D, Collins J, Raisen C, Dyer L, Leung K, Robertson L, Ambridge K, Leongamornlert D, McGuire S, Gilderthorp R, Griffiths C, Manthravadi D, Nichol S, Barker G, Whitehead S, Kay M, Brown J, Murnane C, Gray E, Humphries M, Sycamore N, Barker D, Saunders D, Wallis J, Babbage A, Hammond S, Mashreghi-Mohammadi M, Barr L, Martin S, Wray P, Ellington A, Matthews N, Ellwood M, Woodmansey R, Clark G, Cooper J, Tromans A, Grafham D, Skuce C, Pandian R, Andrews R, Harrison E, Kimberley A, Garnett J, Fosker N, Hall R, Garner P, Kelly D, Bird C, Palmer S, Gehring I, Berger A, Dooley CM, Ersan-Urun Z, Eser C, Geiger H, Geisler M, Karotki L, Kirn A, Konantz J, Konantz M, Oberlander M, Rudolph-Geiger S, Teucke M, Lanz C, Raddatz G, Osoegawa K, Zhu B, Rapp A, Widaa S, Langford C, Yang F, Schuster SC, Carter NP, Harrow J, Ning Z, Herrero J, Searle SM, Enright A, Geisler R, Plasterk RH, Lee C, Westerfield M, de Jong PJ, Zon LI, Postlethwait JH, Nusslein-Volhard C, Hubbard TJ, Roest Crollius H, Rogers J, Stemple DL (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496(7446):498–503. https://doi.org/10.1038/nature12111
Hultman KA, Bahary N, Zon LI, Johnson SL (2007) Gene Duplication of the zebrafish kit ligand and partitioning of melanocyte development functions to kit ligand. PLoS Genet 3(1):e17. https://doi.org/10.1371/journal.pgen.0030017
Inaba M, Yamanaka H, Kondo S (2012) Pigment pattern formation by contact-dependent depolarization. Science 335(6069):677. https://doi.org/10.1126/science.1212821
Inaba M, Jiang TX, Liang YC, Tsai S, Lai YC, Widelitz RB, Chuong CM (2019) Instructive role of melanocytes during pigment pattern formation of the avian skin. Proc Natl Acad Sci U S A 116(14):6884–6890. https://doi.org/10.1073/pnas.1816107116
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(2):190–200. https://doi.org/10.1111/pcmr.12192
Irion U, Frohnhofer HG, Krauss J, Colak Champollion T, Maischein HM, Geiger-Rudolph S, Weiler C, Nusslein-Volhard C (2014) Gap junctions composed of connexins 41.8 and 39.4 are essential for colour pattern formation in zebrafish. elife 3:e05125. https://doi.org/10.7554/eLife.05125
Irion U, Singh AP, Nusslein-Volhard C (2016) The developmental genetics of vertebrate color pattern formation: lessons from zebrafish. Curr Top Dev Biol 117:141–169. https://doi.org/10.1016/bs.ctdb.2015.12.012
Iwashita M, Watanabe M, Ishii M, Chen T, Johnson SL, Kurachi Y, Okada N, Kondo S (2006) Pigment pattern in jaguar/obelix zebrafish is caused by a Kir7.1 mutation: Implications for the regulation of melanosome movement. PLoS Genet 2(11):1861–1870. https://doi.org/10.1371/journal.pgen.0020197
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(6):631–643. https://doi.org/10.1016/j.devcel.2015.04.025
Jacobs LC, Wollstein A, Lao O, Hofman A, Klaver CC, Uitterlinden AG, Nijsten T, Kayser M, Liu F (2013) Comprehensive candidate gene study highlights UGT1A and BNC2 as new genes determining continuous skin color variation in Europeans. Hum Genet 132(2):147–158. https://doi.org/10.1007/s00439-012-1232-9
Jeffery WR (2009) Regressive evolution in Astyanax cavefish. Annu Rev Genet 43:25–47. https://doi.org/10.1146/annurev-genet-102108-134216
Johnson SL, Africa D, Walker C, Weston JA (1995) Genetic control of adult pigment stripe development in zebrafish. Dev Biol 167(1):27–33. https://doi.org/10.1006/dbio.1995.1004
Kapp FG, Perlin JR, Hagedorn EJ, Gansner JM, Schwarz DE, O'Connell LA, Johnson NS, Amemiya C, Fisher DE, Wolfle U, Trompouki E, Niemeyer CM, Driever W, Zon LI (2018) Protection from UV light is an evolutionarily conserved feature of the haematopoietic niche. Nature 558(7710):445–448. https://doi.org/10.1038/s41586-018-0213-0
Kelsh RN, Brand M, Jiang Y-J, Heisenberg C-P, Lin S, Haffter P, Odenthal J, Mullins MC, van Eeden FJM, Furutani-Seiki M, Granato M, Hammerschmidt M, Kane DA, Warga RM, Beuchle D, Vogelsang L, Nusslein-Volhard C (1996) Zebrafish pigmentation mutations and the processes of neural crest development. Development 123:369–389
Kelsh RN, Harris ML, Colanesi S, Erickson CA (2009) Stripes and belly-spots-A review of pigment cell morphogenesis in vertebrates. Semin Cell Dev Biol 20:90–104
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203(3):253–310. https://doi.org/10.1002/aja.1002030302
Kimura T, Nagao Y, Hashimoto H, Yamamoto-Shiraishi Y, Yamamoto S, Yabe T, Takada S, Kinoshita M, Kuroiwa A, Naruse K (2014) Leucophores are similar to xanthophores in their specification and differentiation processes in medaka. Proc Natl Acad Sci U S A 111(20):7343–7348. https://doi.org/10.1073/pnas.1311254111
Kimura T, Takehana Y, Naruse K (2017) pnp4a is the causal gene of the medaka iridophore mutant guanineless. G3 (Bethesda) 7(4):1357–1363. https://doi.org/10.1534/g3.117.040675
Klaassen H, Wang Y, Adamski K, Rohner N, Kowalko JE (2018) CRISPR mutagenesis confirms the role of oca2 in melanin pigmentation in Astyanax mexicanus. Dev Biol 441(2):313–318. https://doi.org/10.1016/j.ydbio.2018.03.014
Kleinjan DA, Bancewicz RM, Gautier P, Dahm R, Schonthaler HB, Damante G, Seawright A, Hever AM, Yeyati PL, van Heyningen V, Coutinho P (2008) Subfunctionalization of duplicated zebrafish pax6 genes by cis-regulatory divergence. PLoS Genet 4(2):e29. https://doi.org/10.1371/journal.pgen.0040029
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(3):631–646. https://doi.org/10.1534/genetics.113.151738
Kratochwil CF, Liang Y, Gerwin J, Woltering JM, Urban S, Henning F, Machado-Schiaffino G, Hulsey CD, Meyer A (2018) Agouti-related peptide 2 facilitates convergent evolution of stripe patterns across cichlid fish radiations. Science 362(6413):457–460. https://doi.org/10.1126/science.aao6809
Kratochwil CF, Urban S, Meyer A (2019) Genome of the Malawi golden cichlid fish (Melanochromis auratus) reveals exon loss of oca2 in an amelanistic morph. Pigment Cell Melanoma Res 32(5):719–723. https://doi.org/10.1111/pcmr.12799
Kurokawa T, Murashita K, Uji S (2006) Characterization and tissue distribution of multiple agouti-family genes in pufferfish, Takifugu rubripes. Peptides 27(12):3165–3175. https://doi.org/10.1016/j.peptides.2006.09.013
Lamason RL, Mohideen MA, Mest JR, Wong AC, Norton HL, Aros MC, Jurynec MJ, Mao X, Humphreville VR, Humbert JE, Sinha S, Moore JL, Jagadeeswaran P, Zhao W, Ning G, Makalowska I, McKeigue PM, O'Donnell D, Kittles R, Parra EJ, Mangini NJ, Grunwald DJ, Shriver MD, Canfield VA, Cheng KC (2005) SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science 310(5755):1782–1786. https://doi.org/10.1126/science.1116238
Lambert MJ, Cochran WO, Wilde BM, Olsen KG, Cooper CD (2015) Evidence for widespread subfunctionalization of splice forms in vertebrate genomes. Genome Res 25(5):624–632. https://doi.org/10.1101/gr.184473.114
Lamoreux ML, Kelsh RN, Wakamatsu Y, Ozato K (2005) Pigment pattern formation in the medaka embryo. Pigment Cell Res 18(2):64–73. https://doi.org/10.1111/j.1600-0749.2005.00216.x
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(11):e1000744. https://doi.org/10.1371/journal.pgen.1000744
Le Douarin NM, Dupin E (2018) The beginnings of the neural crest. Dev Biol. https://doi.org/10.1016/j.ydbio.2018.07.019
Lewis VM, Saunders LM, Larson TA, Bain EJ, Sturiale SL, Gur D, Chowdhury S, Flynn JD, Allen MC, Deheyn DD, Lee JC, Simon JA, Lippincott-Schwartz J, Raible DW, Parichy DM (2019) Fate plasticity and reprogramming in genetically distinct populations of Danio leucophores. Proc Natl Acad Sci 16(24):11806–11811
Li IJ, Chang CJ, Liu SC, Abe G, Ota KG (2015) Postembryonic staging of wild-type goldfish, with brief reference to skeletal systems. Dev Dyn 244(12):1485–1518. https://doi.org/10.1002/dvdy.24340
Liang Y, Gerwin J, Meyer A, Kratochwil CF (2020) Developmental and cellular basis of vertical bar color patterns in the east african cichlid fish Haplochromis latifasciatus. Front Cell Dev Biol 8:62. https://doi.org/10.3389/fcell.2020.00062
Lister JA (2019) Larval but not adult xanthophore pigmentation in zebrafish requires GTP cyclohydrolase 2 (gch2) function. Pigment Cell Melanoma Res 32:724–727. https://doi.org/10.1111/pcmr.12783
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(17):3757–3767
Lopes SS, Yang X, Muller J, Carney TJ, McAdow AR, Rauch GJ, Jacoby AS, Hurst LD, Delfino-Machin M, Haffter P, Geisler R, Johnson SL, Ward A, Kelsh RN (2008) Leukocyte tyrosine kinase functions in pigment cell development. PLoS Genet 4(3):e1000026. https://doi.org/10.1371/journal.pgen.1000026
Lorin T, Brunet FG, Laudet V, Volff JN (2018) Teleost fish-specific preferential retention of pigmentation gene-containing families after whole genome duplications in vertebrates. G3 (Bethesda) 8(5):1795–1806. https://doi.org/10.1534/g3.118.200201
Losey GS, Cronin TW, Goldsmith TH, Hyde D, Marshall NJ, McFarland WN (1999) The UV visual world of fishes: a review. J Fish Biol 54(5):921–943. https://doi.org/10.1111/j.1095-8649.1999.tb00848.x
Maan ME, Sefc KM (2013) Colour variation in cichlid fish: developmental mechanisms, selective pressures and evolutionary consequences. Semin Cell Dev Biol 24(6-7):516–528. https://doi.org/10.1016/j.semcdb.2013.05.003
Mahalwar P, Walderich B, Singh AP, Nusslein-Volhard C (2014) Local reorganization of xanthophores fine-tunes and colors the striped pattern of zebrafish. Science 345(6202):1362–1364. https://doi.org/10.1126/science.1254837
Mahalwar P, Singh AP, Fadeev A, Nusslein-Volhard C, Irion U (2016) Heterotypic interactions regulate cell shape and density during color pattern formation in zebrafish. Biol Open 5(11):1680–1690. https://doi.org/10.1242/bio.022251
Manceau M, Domingues VS, Mallarino R, Hoekstra HE (2011) The developmental role of Agouti in color pattern evolution. Science 331(6020):1062–1065. https://doi.org/10.1126/science.1200684
Marletaz F, Firbas PN, Maeso I, Tena JJ, Bogdanovic O, Perry M, Wyatt CDR, de la Calle-Mustienes E, Bertrand S, Burguera D, Acemel RD, van Heeringen SJ, Naranjo S, Herrera-Ubeda C, Skvortsova K, Jimenez-Gancedo S, Aldea D, Marquez Y, Buono L, Kozmikova I, Permanyer J, Louis A, Albuixech-Crespo B, Le Petillon Y, Leon A, Subirana L, Balwierz PJ, Duckett PE, Farahani E, Aury JM, Mangenot S, Wincker P, Albalat R, Benito-Gutierrez E, Canestro C, Castro F, D'Aniello S, Ferrier DEK, Huang S, Laudet V, Marais GAB, Pontarotti P, Schubert M, Seitz H, Somorjai I, Takahashi T, Mirabeau O, Xu A, Yu JK, Carninci P, Martinez-Morales JR, Crollius HR, Kozmik Z, Weirauch MT, Garcia-Fernandez J, Lister R, Lenhard B, Holland PWH, Escriva H, Gomez-Skarmeta JL, Irimia M (2018) Amphioxus functional genomics and the origins of vertebrate gene regulation. Nature 564(7734):64–70. https://doi.org/10.1038/s41586-018-0734-6
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
McClintock JM, Carlson R, Mann DM, Prince VE (2001) Consequences of Hox gene duplication in the vertebrates: an investigation of the zebrafish Hox paralogue group 1 genes. Development 128(13):2471–2484
McGuirl MR, Volkening A, Sandstede B (2020) Topological data analysis of zebrafish patterns. Proc Natl Acad Sci U S A 117(10):5113–5124. https://doi.org/10.1073/pnas.1917763117
McKinney ML, McNamara KJ (1991) Heterochrony: the evolution of ontogeny. Plenum Press, New York
McMenamin SK, Parichy DM (2013) Metamorphosis in teleosts. Curr Top Dev Biol 103:127–165. https://doi.org/10.1016/B978-0-12-385979-2.00005-8
McMenamin SK, Bain EJ, McCann AE, Patterson LB, Eom DS, Waller ZP, Hamill JC, Kuhlman JA, Eisen JS, Parichy DM (2014) Thyroid hormone-dependent adult pigment cell lineage and pattern in zebrafish. Science 345(6202):1358–1361. https://doi.org/10.1126/science.1256251
Miller CT, Beleza S, Pollen AA, Schluter D, Kittles RA, Shriver MD, Kingsley DM (2007) cis-Regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131(6):1179–1189. https://doi.org/10.1016/j.cell.2007.10.055
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(6):1081–1090. https://doi.org/10.1242/dev.02799
Minchin JE, Hughes SM (2008) Sequential actions of Pax3 and Pax7 drive xanthophore development in zebrafish neural crest. Dev Biol 317(2):508–522. https://doi.org/10.1016/j.ydbio.2008.02.058
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. Proc Natl Acad Sci U S A 114(45):12027–12032. https://doi.org/10.1073/pnas.1710254114
Mundy NI, Kelly J, Theron E, Hawkins K (2003) Evolutionary genetics of the melanocortin-1 receptor in vertebrates. Ann N Y Acad Sci 994:307–312
Nagao Y, Suzuki T, Shimizu A, Kimura T, Seki R, Adachi T, Inoue C, Omae Y, Kamei Y, Hara I, Taniguchi Y, Naruse K, Wakamatsu Y, Kelsh RN, Hibi M, Hashimoto H (2014) Sox5 functions as a fate switch in medaka pigment cell development. PLoS Genet 10(4):e1004246. https://doi.org/10.1371/journal.pgen.1004246
Nagao Y, Takada H, Miyadai M, Adachi T, Seki R, Kamei Y, Hara I, Taniguchi Y, Naruse K, Hibi M, Kelsh RN, Hashimoto H (2018) Distinct interactions of Sox5 and Sox10 in fate specification of pigment cells in medaka and zebrafish. PLoS Genet 14(4):e1007260. https://doi.org/10.1371/journal.pgen.1007260
Nakamasu A, Takahashi G, Kanbe A, Kondo S (2009) Interactions between zebrafish pigment cells responsible for the generation of Turing patterns. Proc Natl Acad Sci U S A 106(21):8429–8434
Nakayama T, Nakajima K, Cox A, Fisher M, Howell M, Fish MB, Yaoita Y, Grainger RM (2017) No privacy, a Xenopus tropicalis mutant, is a model of human Hermansky-Pudlak Syndrome and allows visualization of internal organogenesis during tadpole development. Dev Biol 426(2):472–486. https://doi.org/10.1016/j.ydbio.2016.08.020
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(11):1853–1862. https://doi.org/10.1091/mbc.E15-12-0821
O’Reilly-Pol T, Johnson SL (2008) Melanocyte regeneration reveals mechanisms of adult stem cell regulation. Semin Cell Dev Biol 20(1):117–124
O’Reilly-Pol T, Johnson SL (2013) Kit signaling is involved in melanocyte stem cell fate decisions in zebrafish embryos. Development 140(5):996–1002. https://doi.org/10.1242/dev.088112
Odenthal J, Rossnagel K, Haffter P, Kelsh RN, Vogelsang E, Brand M, van Eeden FJ, Furutani-Seiki M, Granato M, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Mullins MC, Nusslein-Volhard C (1996a) Mutations affecting xanthophore pigmentation in the zebrafish, Danio rerio. Development 123:391–398
Odenthal J, Rossnagel K, Haffter P, Kelsh RN, Vogelsang E, Brand M, van Eeden FJM, Furutani-Seiki M, Granato M, Hammerschmidt C-P, Jiang Y-J, Kane DA, Kelsh RN, Mullins MC, Nusslein-Volhard C (1996b) Mutations affecting xanthophore pigmentation in the zebrafish, Danio rerio. Development 123:391–398
Ohno S (1970) Duplication of regulatory genes and receptors. In: Evolution by gene duplication. Springer, Berlin, pp 82–88
Oliphant LW, Hudon J (1993) Pteridines as reflecting pigments and components of reflecting organelles in vertebrates. Pigment Cell Res 6(4 Pt 1):205–208
Orton GL (1953) Development and migration of pigment cells in some teleost fishes. J Morphol 93:69–99
Owen JP, Kelsh RN, Yates CA (2020) A quantitative modelling approach to zebrafish pigment pattern formation. elife 9:e52998. https://doi.org/10.7554/eLife.52998
Parichy DM (1996) Salamander pigment patterns: how can they be used to study developmental mechanisms and their evolutionary transformation? Int J Dev Biol 40(4):871–884
Parichy DM (1998) Experimental analysis of character coupling across a complex life cycle: pigment pattern metamorphosis in the tiger salamander, Ambystoma tigrinum tigrinum. J Morphol 237(1):53–67
Parichy DM, Spiewak JE (2015) Origins of adult pigmentation: diversity in pigment stem cell lineages and implications for pattern evolution. Pigment Cell Melanoma Res 28(1):31–50. https://doi.org/10.1111/pcmr.12332
Parichy DM, Turner JM (2003a) Cellular interactions during adult pigment stripe development in zebrafish. Academic, New York, p 486
Parichy DM, Turner JM (2003b) Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development. Development 130(5):817–833. https://doi.org/10.1242/dev.00307
Parichy DM, Turner JM (2003c) Zebrafish puma mutant decouples pigment pattern and somatic metamorphosis. Dev Biol 256(2):242–257. https://doi.org/10.1016/s0012-1606(03)00015-0
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(15):3425–3436
Parichy DM, Mellgren EM, Rawls JF, Lopes SS, Kelsh RN, Johnson SL (2000a) Mutational analysis of endothelin receptor b1 (rose) during neural crest and pigment pattern development in the zebrafish Danio rerio. Dev Biol 227(2):294–306. https://doi.org/10.1006/dbio.2000.9899
Parichy DM, Ransom DG, Paw B, Zon LI, Johnson SL (2000b) 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(14):3031–3044
Parichy DM, Reedy MV, Erickson CA (2006) Chapter 5. Regulation of melanoblast migration and differentiation. In: Nordland JJ, Boissy RE, Hearing VJ, King RA, Oetting WS, Ortonne JP (eds) The pigmentary system: physiology and pathophysiology, 2nd edn. Oxford University Press, New York
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
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(5):e1003561. https://doi.org/10.1371/journal.pgen.1003561
Patterson LB, Parichy DM (2019) Zebrafish pigment pattern formation: insights into the development and evolution of adult form. Annu Rev Genet 53:043741. https://doi.org/10.1146/annurev-genet-112618-043741
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. https://doi.org/10.1038/ncomms6299
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(10):e1007402. https://doi.org/10.1371/journal.pgen.1007402
Prazdnikov DV, Shkil FN (2019) Experimental evidence of the role of heterochrony in evolution of the Mesoamerican cichlids pigment patterns. Evol Dev 21(1):3–15
Price AC, Weadick CJ, Shim J, Rodd FH (2008) Pigments, patterns, and fish behavior. Zebrafish 5(4):297–307. https://doi.org/10.1089/zeb.2008.0551
Prince VE, Pickett FB (2002) Splitting pairs: the diverging fates of duplicated genes. Nat Rev Genet 3(11):827–837. https://doi.org/10.1038/nrg928
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(1):107–111
Quigley IK, Turner JM, Nuckels RJ, Manuel JL, Budi EH, MacDonald EL, Parichy DM (2004) Pigment pattern evolution by differential deployment of neural crest and post-embryonic melanophore lineages in Danio fishes. Development 131(24):6053–6069. https://doi.org/10.1242/dev.01526
Quigley IK, Manuel JL, Roberts RA, Nuckels RJ, Herrington ER, MacDonald EL, Parichy DM (2005) Evolutionary diversification of pigment pattern in Danio fishes: differential fms dependence and stripe loss in D. albolineatus. Development 132(1):89–104. https://doi.org/10.1242/dev.01547
Rawles ME (1948) Origin of melanophores and their role in development of color patterns in vertebrates. Physiol Rev 28:383–408
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(1):152–161
Ré P, Meneses I (2008) Early stages of marine fishes occuring in the Iberian peninsula. IPIMAR, Isabel Meneses
Rican O, Musilova Z, Muska M, Novak J (2005) Development of coloration patterns in neotropical cichlids (Teleostei: Cichlidae: Cichlasomatinae). Folia Zool 54:1–46
Rican O, Pialek L, Dragova K, Novak J (2016) Diversity and evolution of the Middle American cichlid fishes (Teleostei: Cichlidae) with revised classification. Vertebr Zool 66(1):3–102
Riddle MR, Aspiras AC, Gaudenz K, Peuss R, Sung JY, Martineau B, Peavey M, Box AC, Tabin JA, McGaugh S, Borowsky R, Tabin CJ, Rohner N (2018) Insulin resistance in cavefish as an adaptation to a nutrient-limited environment. Nature 555(7698):647–651. https://doi.org/10.1038/nature26136
Roberts RB, Ser JR, Kocher TD (2009) Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science 326(5955):998–1001. https://doi.org/10.1126/science.1174705
Roberts RB, Moore EC, Kocher TD (2017) An allelic series at pax7a is associated with colour polymorphism diversity in Lake Malawi cichlid fish. Mol Ecol 26(10):2625–2639. https://doi.org/10.1111/mec.13975
Rosenthal GG (2007) Spatiotemporal dimensions of visual signals in animal communication. Annu Rev Ecol Evol Syst 38:155–178. https://doi.org/10.1146/annurev.ecolsys.38.091206.095745
Roux N, Salis P, Lambert A, Logeux V, Soulat O, Romans P, Frederich B, Lecchini D, Laudet V (2019) Staging and normal table of postembryonic development of the clownfish (Amphiprion ocellaris). Dev Dyn 248(7):545–568. https://doi.org/10.1002/dvdy.46
Saenko SV, Teyssier J, van der Marel D, Milinkovitch MC (2013) Precise colocalization of interacting structural and pigmentary elements generates extensive color pattern variation in Phelsuma lizards. BMC Biol 11:105. https://doi.org/10.1186/1741-7007-11-105
Saldana-Caboverde A, Kos L (2010) Roles of endothelin signaling in melanocyte development and melanoma. Pigment Cell Melanoma Res 23(2):160–170. https://doi.org/10.1111/j.1755-148X.2010.00678.x
Salis P, Roux N, Soulat O, Lecchini D, Laudet V, Frederich B (2018) Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes. BMC Biol 16(1):90. https://doi.org/10.1186/s12915-018-0559-7
Salis P, Lorin T, Lewis V, Rey C, Marcionetti A, Escande ML, Roux N, Besseau L, Salamin N, Semon M, Parichy D, Volff JN, Laudet V (2019) Developmental and comparative transcriptomic identification of iridophore contribution to white barring in clownfish. Pigment Cell Melanoma Res 32:391–402. https://doi.org/10.1111/pcmr.12766
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. https://doi.org/10.1186/1741-7007-5-51
Santos ME, Braasch I, Boileau N, Meyer BS, Sauteur L, Bohne A, Belting HG, Affolter M, Salzburger W (2014) The evolution of cichlid fish egg-spots is linked with a cis-regulatory change. Nat Commun 5:5149. https://doi.org/10.1038/ncomms6149
Saunders LM, Aman AJ, Mishra AK, Lewis VM, Toomey MB, Packer JS, Qiu X, McFaline-Figueroa JL, Corbo JC, Trapnell C, Parichy DM (2019) Thyroid hormone regulates distinct paths to maturation in pigment cell lineages. elife 8:e45181
Sawada R, Aramaki T, Kondo S (2018) Flexibility of pigment cell behavior permits the robustness of skin pattern formation. Genes Cells 23(7):537–545. https://doi.org/10.1111/gtc.12596
Schartl M, Larue L, Goda M, Bosenberg MW, Hashimoto H, Kelsh RN (2016) What is a vertebrate pigment cell? Pigment Cell Melanoma Res 29(1):8–14. https://doi.org/10.1111/pcmr.12409
Schneider RA, Helms JA (2003) The cellular and molecular origins of beak morphology. Science 299(5606):565–568
Seehausen O, Mayhew PJ, Van Alphen JJM (1999) Evolution of colour patterns in East African cichlid fish. J Evol Biol 12(3):514–534
Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, 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(7213):620–626. https://doi.org/10.1038/nature07285
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(1-2):114–122. https://doi.org/10.1016/j.gene.2007.07.005
Shainer I, Michel M, Marquart GD, Bhandiwad AA, Zmora N, Ben-Moshe Livne Z, Zohar Y, Hazak A, Mazon Y, Forster D, Hollander-Cohen L, Cone RD, Burgess HA, Gothilf Y (2019) Agouti-related protein 2 is a new player in the teleost stress response system. Curr Biol 29(12):2009–2019. https://doi.org/10.1016/j.cub.2019.05.021
Singh AP, Schach U, Nusslein-Volhard C (2014) Proliferation, dispersal and patterned aggregation of iridophores in the skin prefigure striped colouration of zebrafish. Nat Cell Biol 16(6):607–614. https://doi.org/10.1038/ncb2955
Singh AP, Dinwiddie A, Mahalwar P, Schach U, Linker C, Irion U, Nusslein-Volhard C (2016) Pigment cell progenitors in zebrafish remain multipotent through metamorphosis. Dev Cell 38(3):316–330. https://doi.org/10.1016/j.devcel.2016.06.020
Spiewak JE, Bain EJ, Liu J, Kou K, Sturiale SL, Patterson LB, Diba P, Eisen JS, Braasch I, Ganz J, Parichy DM (2018) Evolution of endothelin signaling and diversification of adult pigment pattern in Danio fishes. PLoS Genet 14(9):e1007538. https://doi.org/10.1371/journal.pgen.1007538
Streelman JT, Albertson RC, Kocher TD (2003) Genome mapping of the orange blotch colour pattern in cichlid fishes. Mol Ecol 12(9):2465–2471. https://doi.org/10.1046/j.1365-294x.2003.01920.x
Sturm RA, Duffy DL, Box NF, Newton RA, Shepherd AG, Chen W, Marks LH, Leonard JH, Martin NG (2003) Genetic association and cellular function of MC1R variant alleles in human pigmentation. Ann N Y Acad Sci 994:348–358
Svetic V, Hollway GE, Elworthy S, Chipperfield TR, Davison C, Adams RJ, Eisen JS, Ingham PW, Currie PD, Kelsh RN (2007) Sdf1a patterns zebrafish melanophores and links the somite and melanophore pattern defects in choker mutants. Development 134(5):1011–1022. https://doi.org/10.1242/dev.02789
Tadokoro R, Shikaya Y, Takahashi Y (2019) Wide coverage of the body surface by melanocyte-mediated skin pigmentation. Dev Biol 449(2):83–89. https://doi.org/10.1016/j.ydbio.2018.04.016
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(6):677–686. https://doi.org/10.1111/j.1755-148X.2008.00504.x
Tryon RC, Higdon CW, Johnson SL (2011) Lineage relationship of direct-developing melanocytes and melanocyte stem cells in the zebrafish. PLoS ONE 6(6):e21010. https://doi.org/10.1371/journal.pone.0021010
Twitty VC, Bodenstein D (1939) Correlated genetic and embryological experiments on Triturus. J Exp Zool 81:357–398
Urban S, Nater A, Meyer A, Kratochwil CF (2020) Different sources of allelic variation drove repeated color pattern divergence in cichlid fishes. Mol Biol Evol. https://doi.org/10.1093/molbev/msaa237
Usui Y, Aramaki T, Kondo S, Watanabe M (2019) The minimal gap-junction network among melanophores and xanthophores required for stripe pattern formation in zebrafish. Development 146(22). https://doi.org/10.1242/dev.181065
Volkening A, Sandstede B (2015) Modelling stripe formation in zebrafish: an agent-based approach. J R Soc 12:112. https://doi.org/10.1098/rsif.2015.0812
Volkening A, Sandstede B (2018) Iridophores as a source of robustness in zebrafish stripes and variability in Danio patterns. Nat Commun 9(1):3231. https://doi.org/10.1038/s41467-018-05629-z
Volkening A, Abbott MR, Chandra N, Dubois B, Lim F, Sexton D, Sandstede B (2020) Modeling stripe formation on growing zebrafish tailfins. Bull Math Biol 82(5):56. https://doi.org/10.1007/s11538-020-00731-0
Wake DB, Wake MH, Specht CD (2011) Homoplasy: from detecting pattern to determining process and mechanism of evolution. Science 331(6020):1032. https://doi.org/10.1126/science.1188545
Walderich B, Singh AP, Mahalwar P, Nusslein-Volhard C (2016) Homotypic cell competition regulates proliferation and tiling of zebrafish pigment cells during colour pattern formation. Nat Commun 7:11462. https://doi.org/10.1038/ncomms11462
Watanabe M, Kondo S (2015) Is pigment patterning in fish skin determined by the Turing mechanism? Trends Genet 31(2):88–96. https://doi.org/10.1016/j.tig.2014.11.005
Watanabe M, Iwashita M, Ishii M, Kurachi Y, Kawakami A, Kondo S, Okada N (2006) Spot pattern of leopard Danio is caused by mutation in the zebrafish connexin41.8 gene. EMBO Rep 7(9):893–897. https://doi.org/10.1038/sj.embor.7400757
Watanabe K, Washio Y, Fujinami Y, Aritaki M, Uji S, Suzuki T (2008) Adult-type pigment cells, which color the ocular sides of flounders at metamorphosis, localize as precursor cells at the proximal parts of the dorsal and anal fins in early larvae. Develop Growth Differ 50(9):731–741
Watanabe M, Watanabe D, Kondo S (2012) Polyamine sensitivity of gap junctions is required for skin pattern formation in zebrafish. Sci Rep 2:473. https://doi.org/10.1038/srep00473
Woodcock MR, Vaughn-Wolfe J, Elias A, Kump DK, Kendall KD, Timoshevskaya N, Timoshevskiy V, Perry DW, Smith JJ, Spiewak JE, Parichy DM, Voss SR (2017) Identification of mutant genes and introgressed tiger salamander DNA in the laboratory axolotl, Ambystoma mexicanum. Sci Rep 7(1):6. https://doi.org/10.1038/s41598-017-00059-1
Yamada T, Okauchi M, Araki K (2010) Origin of adult-type pigment cells forming the asymmetric pigment pattern, in Japanese flounder (Paralichthys olivaceus). Dev Dyn 239(12):3147–3162. https://doi.org/10.1002/dvdy.22440
Yamaguchi M, Yoshimoto E, Kondo S (2007) Pattern regulation in the stripe of zebrafish suggests an underlying dynamic and autonomous mechanism. Proc Natl Acad Sci U S A 104(12):4790–4793
Yamanaka H, Kondo S (2014) In vitro analysis suggests that difference in cell movement during direct interaction can generate various pigment patterns in vivo. Proc Natl Acad Sci U S A 111(5):1867–1872. https://doi.org/10.1073/pnas.1315416111
Zhang C, Song Y, Thompson DA, Madonna MA, Millhauser GL, Toro S, Varga Z, Westerfield M, Gamse J, Chen W, Cone RD (2010) Pineal-specific agouti protein regulates teleost background adaptation. Proc Natl Acad Sci U S A 107(47):20164–20171. https://doi.org/10.1073/pnas.1014941107
Zhang YM, Zimmer MA, Guardia T, Callahan SJ, Mondal C, Di Martino J, Takagi T, Fennell M, Garippa R, Campbell NR, Bravo-Cordero JJ, White RM (2018) Distant insulin signaling regulates vertebrate pigmentation through the sheddase Bace2. Dev Cell 45(5):580. https://doi.org/10.1016/j.devcel.2018.04.025
Ziegler I (2003) The pteridine pathway in zebrafish: regulation and specification during the determination of neural crest cell-fate. Pigment Cell Res 16(3):172–182
Ziegler I, McDonald T, Hesslinger C, Pelletier I, Boyle P (2000) Development of the pteridine pathway in the zebrafish, Danio rerio. J Biol Chem 275(25):18926–18932. https://doi.org/10.1074/jbc.M910307199
Acknowledgements
DMP and research in his laboratory are supported by NIH R35 GM122471. Images not attributed in figure legends were stock photographs or taken by D. Parichy.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Parichy, D.M., Liang, Y. (2021). Evolution of Pigment Pattern Formation in Teleosts. In: Hashimoto, H., Goda, M., Futahashi, R., Kelsh, R., Akiyama, T. (eds) Pigments, Pigment Cells and Pigment Patterns. Springer, Singapore. https://doi.org/10.1007/978-981-16-1490-3_10
Download citation
DOI: https://doi.org/10.1007/978-981-16-1490-3_10
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-16-1489-7
Online ISBN: 978-981-16-1490-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)