A complex genetic architecture in zebrafish relatives Danio quagga and D. kyathit underlies development of stripes and spots
Autoři:
Braedan M. McCluskey aff001; Susumu Uji aff002; Joseph L. Mancusi aff001; John H. Postlethwait aff003; David M. Parichy aff001
Působiště autorů:
Department of Biology, University of Virginia, Charlottesville, Virginia, United States of America
aff001; Japan Fisheries Research and Education Agency, Watarai, Japan
aff002; Institute of Neuroscience, University of Oregon, Eugene, Oregon, United States of America
aff003; Department of Cell Biology, University of Virginia, Charlottesville, Virginia, United States of America
aff004
Vyšlo v časopise:
A complex genetic architecture in zebrafish relatives Danio quagga and D. kyathit underlies development of stripes and spots. PLoS Genet 17(4): e1009364. doi:10.1371/journal.pgen.1009364
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009364
Souhrn
Vertebrate pigmentation is a fundamentally important, multifaceted phenotype. Zebrafish, Danio rerio, has been a valuable model for understanding genetics and development of pigment pattern formation due to its genetic and experimental tractability, advantages that are shared across several Danio species having a striking array of pigment patterns. Here, we use the sister species D. quagga and D. kyathit, with stripes and spots, respectively, to understand how natural genetic variation impacts phenotypes at cellular and organismal levels. We first show that D. quagga and D. kyathit phenotypes resemble those of wild-type D. rerio and several single locus mutants of D. rerio, respectively, in a morphospace defined by pattern variation along dorsoventral and anteroposterior axes. We then identify differences in patterning at the cellular level between D. quagga and D. kyathit by repeated daily imaging during pattern development and quantitative comparisons of adult phenotypes, revealing that patterns are similar initially but diverge ontogenetically. To assess the genetic architecture of these differences, we employ reduced-representation sequencing of second-generation hybrids. Despite the similarity of D. quagga to D. rerio, and D. kyathit to some D. rerio mutants, our analyses reveal a complex genetic basis for differences between D. quagga and D. kyathit, with several quantitative trait loci contributing to variation in overall pattern and cellular phenotypes, epistatic interactions between loci, and abundant segregating variation within species. Our findings provide a window into the evolutionary genetics of pattern-forming mechanisms in Danio and highlight the complexity of differences that can arise even between sister species. Further studies of natural genetic diversity underlying pattern variation in D. quagga and D. kyathit should provide insights complementary to those from zebrafish mutant phenotypes and more distant species comparisons.
Klíčová slova:
Alleles – Genetic loci – Genomics – Melanophores – Phenotypes – Pigments – Quantitative trait loci – Zebrafish
Zdroje
1. Hamilton F. An Account of the Fishes found in the River Ganges and its Branches. Edinburgh: Archibald Constable and Company; 1822.
2. Cartner SC, Eisen JS, Farmer SC, Guillemin KJ, Kent ML, Sanders GE. The Zebrafish in Biomedical Research: Academic Press; 2020 2020/01/01/.
3. Parichy DM, Elizondo MR, Mills MG, Gordon TN, Engeszer RE. Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish. Developmental Dynamics. 2009;238:2975–3015. doi: 10.1002/dvdy.22113 19891001
4. Patterson LB, Parichy DM. Zebrafish Pigment Pattern Formation: Insights into the Development and Evolution of Adult Form. Annu Rev Genet. 2019;53:505–30. Epub 2019/09/12. doi: 10.1146/annurev-genet-112618-043741 31509458.
5. Irion U, Singh AP, Nusslein-Volhard C. The Developmental Genetics of Vertebrate Color Pattern Formation: Lessons from Zebrafish. Curr Top Dev Biol. 2016;117:141–69. doi: 10.1016/bs.ctdb.2015.12.012 26969976.
6. Gur D, Bain EJ, Johnson KR, Aman AJ, Pasoili HA, Flynn JD, et al. In situ differentiation of iridophore crystallotypes underlies zebrafish stripe patterning. Nat Commun. 2020;11(1):6391. Epub 2020/12/16. doi: 10.1038/s41467-020-20088-1 33319779; PubMed Central PMCID: PMC7738553.
7. Hirata M, Nakamura K, Kanemaru T, Shibata Y, Kondo S. Pigment cell organization in the hypodermis of zebrafish. Dev Dyn. 2003;227(4):497–503. doi: 10.1002/dvdy.10334 12889058.
8. Engeszer RE, Wang G, Ryan MJ, Parichy DM. Sex-specific perceptual spaces for a vertebrate basal social aggregative behavior. Proc Natl Acad Sci U S A. 2008;105(3):929–33. Epub 2008/01/18. doi: 10.1073/pnas.0708778105 18199839; PubMed Central PMCID: PMC2242707.
9. McCann LI, Carlson CC. Effect of cross-rearing on species identification in zebra fish and pearl danios. Dev Psychobiol. 1982;15(1):71–4. doi: 10.1002/dev.420150110 7054017.
10. Lewis VM, Saunders LM, Larson TA, Bain EJ, Sturiale SL, Gur D, et al. Fate plasticity and reprogramming in genetically distinct populations of Danio leucophores. Proc Natl Acad Sci U S A. 2019;116(24):11806–11. Epub 2019/05/30. doi: 10.1073/pnas.1901021116 31138706; PubMed Central PMCID: PMC6575160.
11. Price AC, Weadick CJ, Shim J, Rodd FH. Pigments, patterns, and fish behavior. Zebrafish. 2008;5(4):297–307. doi: 10.1089/zeb.2008.0551 19133828.
12. Negro JJ, Dona J, Blazquez MC, Rodriguez A, Herbert-Read JE, Brooke ML. Contrasting stripes are a widespread feature of group living in birds, mammals and fishes. Proc Biol Sci. 2020;287(1936):20202021. Epub 2020/10/14. doi: 10.1098/rspb.2020.2021 33049169; PubMed Central PMCID: PMC7657865.
13. Endler JA. Natural and sexual selection on color patterns in Poeciliid fishes. Env Biol Fishes. 1983;9:173–90.
14. Marshall NJ, Cortesi F, de Busserolles F, Siebeck UE, Cheney KL. Colours and colour vision in reef fishes: Past, present and future research directions. J Fish Biol. 2018. Epub 2018/10/26. doi: 10.1111/jfb.13849 30357835.
15. Parichy DM. Evolution of pigment cells and patterns: recent insights from teleost fishes. Curr Opin Genet Dev. 2021;69:88–96. Epub 2021/03/21. doi: 10.1016/j.gde.2021.02.006 33743392.
16. McCluskey BM, Postlethwait JH. Phylogeny of Zebrafish, a "Model Species," within Danio, a "Model Genus". Mol Biol Evol. 2015;32(3):635–52. doi: 10.1093/molbev/msu325 25415969; PubMed Central PMCID: PMC4327152.
17. Spiewak JE, Bain EJ, Liu J, Kou K, Sturiale SL, Patterson LB, et al. Evolution of Endothelin signaling and diversification of adult pigment pattern in Danio fishes. PLoS Genet. 2018;14(9):e1007538. Epub 2018/09/19. doi: 10.1371/journal.pgen.1007538 30226839; PubMed Central PMCID: PMC6161917.
18. Patterson LB, Bain EJ, Parichy DM. Pigment cell interactions and differential xanthophore recruitment underlying zebrafish stripe reiteration and Danio pattern evolution. Nat Commun. 2014;5:5299. doi: 10.1038/ncomms6299 25374113; PubMed Central PMCID: PMC4224114.
19. Parichy DM. Advancing biology through a deeper understanding of zebrafish ecology and evolution. eLife. 2015;4:e05635. doi: 10.7554/eLife.05635 25807087; PubMed Central PMCID: PMC4373672.
20. Budi EH, Patterson LB, Parichy DM. Post-embryonic nerve-associated precursors to adult pigment cells: genetic requirements and dynamics of morphogenesis and differentiation. PLoS Genet. 2011;7(5):e1002044. Epub 2011/06/01. doi: 10.1371/journal.pgen.1002044 21625562; PubMed Central PMCID: PMC3098192.
21. Singh AP, Dinwiddie A, Mahalwar P, Schach U, Linker C, Irion U, et al. Pigment Cell Progenitors in Zebrafish Remain Multipotent through Metamorphosis. Dev Cell. 2016;38(3):316–30. doi: 10.1016/j.devcel.2016.06.020 27453500.
22. Dooley CM, Mongera A, Walderich B, Nusslein-Volhard C. On the embryonic origin of adult melanophores: the role of ErbB and Kit signalling in establishing melanophore stem cells in zebrafish. Development. 2013;140(5):1003–13. Epub 2013/02/01. doi: 10.1242/dev.087007 23364329.
23. McMenamin SK, Bain EJ, McCann AE, Patterson LB, Eom DS, Waller ZP, et al. Thyroid hormone-dependent adult pigment cell lineage and pattern in zebrafish. Science. 2014;345(6202):1358–61. doi: 10.1126/science.1256251 25170046; PubMed Central PMCID: PMC4211621.
24. Frohnhofer HG, Krauss J, Maischein HM, Nusslein-Volhard C. Iridophores and their interactions with other chromatophores are required for stripe formation in zebrafish. Development. 2013;140(14):2997–3007. Epub 2013/07/04. doi: 10.1242/dev.096719 23821036.
25. Patterson LB, Parichy DM. Interactions with iridophores and the tissue environment required for patterning melanophores and xanthophores during zebrafish adult pigment stripe formation. PLoS Genet. 2013;9(5):e1003561. Epub 2013/06/06. doi: 10.1371/journal.pgen.1003561 23737760; PubMed Central PMCID: PMC3667786.
26. Parichy DM, Turner JM. Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development. Development. 2003;130(5):817–33. doi: 10.1242/dev.00307 12538511.
27. Inoue S, Kondo S, Parichy DM, Watanabe M. Tetraspanin 3c requirement for pigment cell interactions and boundary formation in zebrafish adult pigment stripes. Pigment Cell Melanoma Res. 2014;27(2):190–200. doi: 10.1111/pcmr.12192 24734316; PubMed Central PMCID: PMC3988474.
28. Usui Y, Aramaki T, Kondo S, Watanabe M. The minimal gap-junction network among melanophores and xanthophores required for stripe pattern formation in zebrafish. Development. 2019;146(22). Epub 2019/11/02. doi: 10.1242/dev.181065 31666235.
29. Mahalwar P, Singh AP, Fadeev A, Nusslein-Volhard C, Irion U. Heterotypic interactions regulate cell shape and density during color pattern formation in zebrafish. Biology open. 2016;5(11):1680–90. doi: 10.1242/bio.022251 27742608.
30. Walderich B, Singh AP, Mahalwar P, Nusslein-Volhard C. Homotypic cell competition regulates proliferation and tiling of zebrafish pigment cells during colour pattern formation. Nat Commun. 2016;7:11462. doi: 10.1038/ncomms11462 27118125; PubMed Central PMCID: PMC4853480.
31. Nakamasu A, Takahashi G, Kanbe A, Kondo S. Interactions between zebrafish pigment cells responsible for the generation of Turing patterns. Proc Natl Acad Sci U S A. 2009;106(21):8429–34. Epub 2009/05/13. doi: 10.1073/pnas.0808622106 19433782; PubMed Central PMCID: PMC2689028.
32. Watanabe M, Kondo S. Is pigment patterning in fish skin determined by the Turing mechanism? Trends Genet. 2015;31(2):88–96. doi: 10.1016/j.tig.2014.11.005 25544713.
33. Hamada H, Watanabe M, Lau HE, Nishida T, Hasegawa T, Parichy DM, et al. Involvement of Delta/Notch signaling in zebrafish adult pigment stripe patterning. Development. 2014;141(2):318–24. doi: 10.1242/dev.099804 24306107; PubMed Central PMCID: PMC3879813.
34. Mort RL, Jackson IJ, Patton EE. The melanocyte lineage in development and disease. Development. 2015;142(4):620–32. doi: 10.1242/dev.106567 25670789.
35. Owen JP, Kelsh RN, Yates CA. A quantitative modelling approach to zebrafish pigment pattern formation. eLife. 2020;9. Epub 2020/07/28. doi: 10.7554/eLife.52998 32716296; PubMed Central PMCID: PMC7384860.
36. Volkening A. Linking genotype, cell behavior, and phenotype: multidisciplinary perspectives with a basis in zebrafish patterns. Curr Opin Genet Dev. 2020;63:78–85. Epub 2020/07/01. doi: 10.1016/j.gde.2020.05.010 32604031.
37. Gramann AK, Venkatesan AM, Guerin M, Ceol CJ. Regulation of zebrafish melanocyte development by ligand-dependent BMP signaling. eLife. 2019;8. Epub 2019/12/24. doi: 10.7554/eLife.50047 31868592; PubMed Central PMCID: PMC6968919.
38. Lister JA, Robertson CP, Lepage T, Johnson SL, Raible DW. nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development. 1999;126(17):3757–67. 10433906.
39. Johnson SL, Africa D, Walker C, Weston JA. Genetic control of adult pigment stripe development in zebrafish. Dev Biol. 1995;167(1):27–33. doi: 10.1006/dbio.1995.1004 7851648.
40. Zhang YM, Zimmer MA, Guardia T, Callahan SJ, Mondal C, Di Martino J, et al. Distant Insulin Signaling Regulates Vertebrate Pigmentation through the Sheddase Bace2. Developmental Cell. 2018;45(5):580-+. doi: 10.1016/j.devcel.2018.04.025 WOS:000435092700008. 29804876
41. Nagao Y, Takada H, Miyadai M, Adachi T, Seki R, Kamei Y, et al. Distinct interactions of Sox5 and Sox10 in fate specification of pigment cells in medaka and zebrafish. PLoS Genet. 2018;14(4):e1007260. Epub 2018/04/06. doi: 10.1371/journal.pgen.1007260 29621239; PubMed Central PMCID: PMC5886393.
42. Cal L, Suarez-Bregua P, Comesana P, Owen J, Braasch I, Kelsh R, et al. Countershading in zebrafish results from an Asip1 controlled dorsoventral gradient of pigment cell differentiation. Scientific reports. 2019;9(1):3449. Epub 2019/03/07. doi: 10.1038/s41598-019-40251-z 30837630; PubMed Central PMCID: PMC6401153.
43. Eskova A, Frohnhofer HG, Nusslein-Volhard C, Irion U. Galanin Signaling in the Brain Regulates Color Pattern Formation in Zebrafish. Curr Biol. 2020;30(2):298–303 e3. Epub 2020/01/07. doi: 10.1016/j.cub.2019.11.033 31902721; PubMed Central PMCID: PMC6971688.
44. Endoh M, Shima F, Havelka M, Asanuma R, Yamaha E, Fujimoto T, et al. Hybrid between Danio rerio female and Danio nigrofasciatus male produces aneuploid sperm with limited fertilization capacity. PLoS One. 2020;15(5):e0233885. Epub 2020/05/30. doi: 10.1371/journal.pone.0233885 32470029; PubMed Central PMCID: PMC7259755.
45. Parichy DM, Johnson SL. Zebrafish hybrids suggest genetic mechanisms for pigment pattern diversification in Danio. Dev Genes Evol. 2001;211(7):319–28. doi: 10.1007/s004270100155 11466528.
46. Wong TT, Saito T, Crodian J, Collodi P. Zebrafish germline chimeras produced by transplantation of ovarian germ cells into sterile host larvae. Biol Reprod. 2011;84(6):1190–7. Epub 2011/01/21. doi: 10.1095/biolreprod.110.088427 21248287; PubMed Central PMCID: PMC3099584.
47. Fang F. Danio kyathit, a new species of cyprinid fish from Myitkyina, northern Myanmar. Ichthyol Explor Freshwaters. 1998;8:273–80.
48. Kullander SO, Liao TY, Fang F. Danio quagga, a new species of striped danio from western Myanmar (Teleostei: Cyprinidae). Ichthyol Explor Freshw. 2009;20(3):193–9. WOS:000272708500001.
49. Quigley IK, Manuel JL, Roberts RA, Nuckels RJ, Herrington ER, MacDonald EL, et al. Evolutionary diversification of pigment pattern in Danio fishes: differential fms dependence and stripe loss in D. albolineatus. Development. 2005;132(1):89–104. doi: 10.1242/dev.01547 15563521.
50. Hirata M, Nakamura K, Kondo S. Pigment cell distributions in different tissues of the zebrafish, with special reference to the striped pigment pattern. Dev Dyn. 2005;234(2):293–300. doi: 10.1002/dvdy.20513 16110504.
51. Eom DS, Inoue S, Patterson LB, Gordon TN, Slingwine R, Kondo S, et al. Melanophore migration and survival during zebrafish adult pigment stripe development require the immunoglobulin superfamily adhesion molecule Igsf11. PLoS Genet. 2012;8(8):e1002899. Epub 2012/08/24. doi: 10.1371/journal.pgen.1002899 22916035; PubMed Central PMCID: PMC3420941.
52. Fadeev A, Krauss J, Frohnhofer HG, Irion U, Nusslein-Volhard C. Tight Junction Protein 1a regulates pigment cell organisation during zebrafish colour patterning. eLife. 2015;4. doi: 10.7554/eLife.06545 25915619; PubMed Central PMCID: PMC4446668.
53. Eskova A, Chauvigne F, Maischein HM, Ammelburg M, Cerda J, Nusslein-Volhard C, et al. Gain-of-function mutations in Aqp3a influence zebrafish pigment pattern formation through the tissue environment. Development. 2017;144(11):2059–69. Epub 2017/05/17. doi: 10.1242/dev.143495 28506994; PubMed Central PMCID: PMC5482984.
54. Saunders LM, Mishra AK, Aman AJ, Lewis VM, Toomey MB, Packer JS, et al. Thyroid hormone regulates distinct paths to maturation in pigment cell lineages. Elife. 2019;8. Epub 2019/05/30. doi: 10.7554/eLife.45181 31140974; PubMed Central PMCID: PMC6588384.
55. McClure M, McCune AR. Evidence for developmental linkage of pigment patterns with body size and shape in danios (Teleostei: Cyprinidae). Evolution Int J Org Evolution. 2003;57(8):1863–75. doi: 10.1111/j.0014-3820.2003.tb00594.x 14503628.
56. Volkening A, Sandstede B. Modelling stripe formation in zebrafish: an agent-based approach. Journal of the Royal Society, Interface / the Royal Society. 2015;12(112). doi: 10.1098/rsif.2015.0812 26538560; PubMed Central PMCID: PMC4685853.
57. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One. 2008;3(10):e3376. Epub 2008/10/15. doi: 10.1371/journal.pone.0003376 18852878; PubMed Central PMCID: PMC2557064.
58. JW VANO. Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet Res (Camb). 2011;93(5):343–9. Epub 2011/09/01. doi: 10.1017/S0016672311000279 21878144.
59. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754–60. Epub 2009/05/20. doi: 10.1093/bioinformatics/btp324 19451168; PubMed Central PMCID: PMC2705234.
60. Lamason RL, Mohideen MA, Mest JR, Wong AC, Norton HL, Aros MC, et al. SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science. 2005;310(5755):1782–6. Epub 2005/12/17. doi: 10.1126/science.1116238 16357253.
61. Cal L, Suarez-Bregua P, Braasch I, Irion U, Kelsh R, Cerda-Reverter JM, et al. Loss-of-function mutations in the melanocortin 1 receptor cause disruption of dorso-ventral countershading in teleost fish. Pigment Cell Melanoma Res. 2019;32(6):817–28. Epub 2019/06/30. doi: 10.1111/pcmr.12806 31251842.
62. Parichy DM, Rawls JF, Pratt SJ, Whitfield TT, Johnson SL. 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. 1999;126(15):3425–36. 10393121.
63. Fadeev A, Mendoza-Garcia P, Irion U, Guan J, Pfeifer K, Wiessner S, et al. 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. 2018;115(4):E630–E8. Epub 2018/01/11. doi: 10.1073/pnas.1719137115 29317532; PubMed Central PMCID: PMC5789956.
64. Mo ES, Cheng Q, Reshetnyak AV, Schlessinger J, Nicoli S. 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. 2017;114(45):12027–32. PubMed Central PMCID: PMC5692561. doi: 10.1073/pnas.1710254114 29078341
65. Kottler VA, Fadeev A, Weigel D, Dreyer C. Pigment pattern formation in the guppy, Poecilia reticulata, involves the Kita and Csf1ra receptor tyrosine kinases. Genetics. 2013;194(3):631–46. PubMed Central PMCID: PMC3697969. doi: 10.1534/genetics.113.151738 23666934
66. Giuffra E, Tornsten A, Marklund S, Bongcam-Rudloff E, Chardon P, Kijas JM, et al. A large duplication associated with dominant white color in pigs originated by homologous recombination between LINE elements flanking KIT. Mamm Genome. 2002;13(10):569–77. Epub 2002/11/07. doi: 10.1007/s00335-002-2184-5 12420135.
67. Haase B, Brooks SA, Schlumbaum A, Azor PJ, Bailey E, Alaeddine F, et al. Allelic heterogeneity at the equine KIT locus in dominant white (W) horses. PLoS Genet. 2007;3(11):e195. Epub 2007/11/14. doi: 10.1371/journal.pgen.0030195 17997609; PubMed Central PMCID: PMC2065884.
68. Woodcock MR, Vaughn-Wolfe J, Elias A, Kump DK, Kendall KD, Timoshevskaya N, et al. Identification of Mutant Genes and Introgressed Tiger Salamander DNA in the Laboratory Axolotl, Ambystoma mexicanum. Scientific reports. 2017;7(1):6. doi: 10.1038/s41598-017-00059-1 28127056.
69. Kaelin CB, Xu X, Hong LZ, David VA, McGowan KA, Schmidt-Kuntzel A, et al. Specifying and sustaining pigmentation patterns in domestic and wild cats. Science. 2012;337(6101):1536–41. Epub 2012/09/22. doi: 10.1126/science.1220893 22997338; PubMed Central PMCID: PMC3709578.
70. Li L, Li D, Liu L, Li S, Feng Y, Peng X, et al. Endothelin Receptor B2 (EDNRB2) Gene Is Associated with Spot Plumage Pattern in Domestic Ducks (Anas platyrhynchos). PLoS One. 2015;10(5):e0125883. doi: 10.1371/journal.pone.0125883 25955279; PubMed Central PMCID: PMC4425580.
71. Li Y, Levran O, Kim J, Zhang TJ, Chen XD, Suo C. Extreme sampling design in genetic association mapping of quantitative trait loci using balanced and unbalanced case-control samples. Sci Rep-Uk. 2019;9. doi: 10.1038/s41598-019-51790-w WOS:000493048400057. 31664079
72. Irion U, Frohnhofer HG, Krauss J, Colak Champollion T, Maischein HM, Geiger-Rudolph S, et al. Gap junctions composed of connexins 41.8 and 39.4 are essential for colour pattern formation in zebrafish. eLife. 2014;3:e05125. doi: 10.7554/eLife.05125 25535837; PubMed Central PMCID: PMC4296512.
73. Kratochwil CF, Liang Y, Gerwin J, Woltering JM, Urban S, Henning F, et al. Agouti-related peptide 2 facilitates convergent evolution of stripe patterns across cichlid fish radiations. Science. 2018;362(6413):457–60. Epub 2018/10/27. doi: 10.1126/science.aao6809 30361373.
74. Roberts RB, Ser JR, Kocher TD. Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science. 2009;326(5955):998–1001. doi: 10.1126/science.1174705 19797625; PubMed Central PMCID: PMC3174268.
75. Protas ME, Hersey C, Kochanek D, Zhou Y, Wilkens H, Jeffery WR, et al. Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nat Genet. 2006;38(1):107–11. doi: 10.1038/ng1700 16341223.
76. Watanabe M, Iwashita M, Ishii M, Kurachi Y, Kawakami A, Kondo S, et al. Spot pattern of leopard Danio is caused by mutation in the zebrafish connexin41.8 gene. EMBO Rep. 2006;7(9):893–7. Epub 2006/07/18. doi: 10.1038/sj.embor.7400757 16845369; PubMed Central PMCID: PMC1559663.
77. Steiner CC, Weber JN, Hoekstra HE. Adaptive variation in beach mice produced by two interacting pigmentation genes. PLoS Biol. 2007;5(9):e219. Epub 2007/08/19. doi: 10.1371/journal.pbio.0050219 17696646; PubMed Central PMCID: PMC1945039.
78. Domyan ET, Guernsey MW, Kronenberg Z, Krishnan S, Boissy RE, Vickrey AI, et al. Epistatic and combinatorial effects of pigmentary gene mutations in the domestic pigeon. Curr Biol. 2014;24(4):459–64. Epub 2014/02/11. doi: 10.1016/j.cub.2014.01.020 24508169; PubMed Central PMCID: PMC3990261.
79. Vickrey AI, Bruders R, Kronenberg Z, Mackey E, Bohlender RJ, Maclary ET, et al. Introgression of regulatory alleles and a missense coding mutation drive plumage pattern diversity in the rock pigeon. eLife. 2018;7. Epub 2018/07/18. doi: 10.7554/eLife.34803 30014848; PubMed Central PMCID: PMC6050045.
80. Podobnik M, Frohnhofer HG, Dooley CM, Eskova A, Nusslein-Volhard C, Irion U. Evolution of the potassium channel gene Kcnj13 underlies colour pattern diversification in Danio fish. Nat Commun. 2020;11(1):6230. Epub 2020/12/06. doi: 10.1038/s41467-020-20021-6 33277491; PubMed Central PMCID: PMC7718271.
81. Volkening A, Sandstede B. Iridophores as a source of robustness in zebrafish stripes and variability in Danio patterns. Nat Commun. 2018;9(1):3231. Epub 2018/08/15. doi: 10.1038/s41467-018-05629-z 30104716; PubMed Central PMCID: PMC6089994.
82. Asai R, Taguchi E, Kume Y, Saito M, Kondo S. Zebrafish leopard gene as a component of the putative reaction-diffusion system. Mech Dev. 1999;89(1–2):87–92. doi: 10.1016/s0925-4773(99)00211-7 10559483.
83. LaFave MC, Varshney GK, Vemulapalli M, Mullikin JC, Burgess SM. A Defined Zebrafish Line for High-Throughput Genetics and Genomics: NHGRI-1. Genetics. 2014;198(1):167–70. doi: 10.1534/genetics.114.166769 25009150; PubMed Central PMCID: PMC4174928.
84. Parichy DM. Homology and the evolution of novelty during Danio adult pigment pattern development. J Exp Zoolog B Mol Dev Evol. 2007;308(5):578–90. Epub 2006/11/10. doi: 10.1002/jez.b.21141 17094081.
85. Lopes SS, Yang X, Muller J, Carney TJ, McAdow AR, Rauch GJ, et al. Leukocyte tyrosine kinase functions in pigment cell development. PLoS Genet. 2008;4(3):e1000026. Epub 2008/03/29. doi: 10.1371/journal.pgen.1000026 18369445; PubMed Central PMCID: PMC2265441.
86. Frohnhofer HG, Geiger-Rudolph S, Pattky M, Meixner M, Huhn C, Maischein HM, et al. Spermidine, but not spermine, is essential for pigment pattern formation in zebrafish. Biology open. 2016;5(6):736–44. doi: 10.1242/bio.018721 27215328; PubMed Central PMCID: PMC4920196.
87. Rueden CT, Schindelin J, Hiner MC, DeZonia BE, Walter AE, Arena ET, et al. ImageJ2: ImageJ for the next generation of scientific image data. Bmc Bioinformatics. 2017;18. 52910.1186/s12859-017-1934-z. WOS:000416903700003. doi: 10.1186/s12859-016-1415-9 28056782
88. Adrian Baddeley ER, Rolf Turner. Spatial Point Patterns: Methodology and Applications with R: Chapman and Hall/CRC; 2015. doi: 10.5603/IMH.2015.0010 25792166
89. Tinevez JY, Perry N, Schindelin J, Hoopes GM, Reynolds GD, Laplantine E, et al. TrackMate: An open and extensible platform for single-particle tracking. Methods. 2017;115:80–90. doi: 10.1016/j.ymeth.2016.09.016 WOS:000398010700009. 27713081
90. Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE. Double Digest RADseq: An Inexpensive Method for De Novo SNP Discovery and Genotyping in Model and Non-Model Species. Plos One. 2012;7(5). ARTN e3713510.1371/journal.pone.0037135. WOS:000305338500032. doi: 10.1371/journal.pone.0037135 22675423
91. Xu P, Zhang X, Wang X, Li J, Liu G, Kuang Y, et al. Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nat Genet. 2014;46(11):1212–9. Epub 2014/09/23. doi: 10.1038/ng.3098 25240282.
92. Sola L, Gornung E. Classical and molecular cytogenetics of the zebrafish, Danio rerio (Cyprinidae, Cypriniformes): an overview. Genetica. 2001;111(1–3):397–412. Epub 2002/02/14. doi: 10.1023/a:1013776323077 11841183.
93. Gold JR, Womac WD, Deal FH, Barlow JA. Gross karyotypic change and evolution in North American cyprinid fishes. Genetical Research. 1978;32(1):37–46. Epub 2009/04/14. doi: 10.1017/S0016672300018504
94. Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH. Stacks: Building and Genotyping Loci De Novo From Short-Read Sequences. G3-Genes Genom Genet. 2011;1(3):171–82. doi: 10.1534/g3.111.000240 WOS:000312406900001. 22384329
95. Rochette NC, Rivera-Colon AG, Catchen JM. Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Mol Ecol. 2019;28(21):4737–54. doi: 10.1111/mec.15253 WOS:000490719000001. 31550391
96. Broman KW, Gatti DM, Simecek P, Furlotte NA, Prins P, Sen S, et al. R/qtl2: Software for Mapping Quantitative Trait Loci with High-Dimensional Data and Multiparent Populations. Genetics. 2019;211(2):495–502. doi: 10.1534/genetics.118.301595 WOS:000458574800008. 30591514
97. Prashad B, Mukerji DD. The fish of the Indawgyi Lake and the streams of the Myitkyina District (Upper Burma). Rec Indian Mus. 1929;31:161–223.
98. Parichy DM, Mellgren EM, Rawls JF, Lopes SS, Kelsh RN, Johnson SL. Mutational analysis of endothelin receptor b1 (rose) during neural crest and pigment pattern development in the zebrafish Danio rerio. Dev Biol. 2000;227(2):294–306. doi: 10.1006/dbio.2000.9899 11071756.
99. Parichy DM, Ransom DG, Paw B, Zon LI, Johnson SL. 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. 2000;127(14):3031–44. Epub 2000/06/23. 10862741.
100. Iwashita M, Watanabe M, Ishii M, Chen T, Johnson SL, Kurachi Y, et al. Pigment pattern in jaguar/obelix zebrafish is caused by a Kir7.1 mutation: Implications for the regulation of melanosome movement. Plos Genetics. 2006;2(11):1861–70. doi: 10.1371/journal.pgen.0020197 WOS:000242374600016. 17121467
101. Krauss J, Astrinides P, Frohnhofer HG, Walderich B, Nusslein-Volhard C. transparent, a gene affecting stripe formation in Zebrafish, encodes the mitochondrial protein Mpv17 that is required for iridophore survival. Biology open. 2013;2(7):703–10. Epub 2013/07/19. doi: 10.1242/bio.20135132 23862018; PubMed Central PMCID: PMC3711038.
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