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Assembly of the threespine stickleback Y chromosome reveals convergent signatures of sex chromosome evolution

Catherine L. Peichel, Shaugnessy R. McCann, Joseph A. Ross and 8 more

Genome Biology · 2020 · CC BY

doi:10.1101/2019.12.12.874701

Abstract

Background. Heteromorphic sex chromosomes have evolved repeatedly across diverse species. Suppression of recombination between X and Y chromosomes leads to degeneration of the Y chromosome. The progression of degeneration is not well understood, as complete sequence assemblies of heteromorphic Y chromosomes have only been generated across a handful of taxa with highly degenerate sex chromosomes. Here, we describe the assembly of the threespine stickleback (Gasterosteus aculeatus) Y chromosome, which is less than 26 million years old and at an intermediate stage of degeneration. Our previous work identified that the non-recombining region between the X and the Y spans approximately 17.5 Mb on the X chromosome.

Results. We combine long-read sequencing with a Hi-C-based proximity guided assembly to generate a 15.87 Mb assembly of the Y chromosome. Our assembly is concordant with cytogenetic maps and Sanger sequences of over 90 Y chromosome BAC clones. We find three evolutionary strata on the Y chromosome, consistent with the three inversions identified by our previous cytogenetic analyses. The threespine stickleback Y shows convergence with more degenerate sex chromosomes in the retention of haploinsufficient genes and the accumulation of genes with testis-biased expression, many of which are recent duplicates. However, we find no evidence for large amplicons identified in other sex chromosome systems. We also report an excellent candidate for the master sex-determination gene: a translocated copy of Amh (Amhy).

Conclusions. Together, our work shows that the evolutionary forces shaping sex chromosomes can cause relatively rapid changes in the overall genetic architecture of Y chromosomes.

References 139

  1. 1.

    Bachtrog D. Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet. 2013;14:113-124.

    Not in our library10.1038/nrg3366

  2. 2.
    Sex Determination: Why So Many Ways of Doing It? · 2014
    No notice
  3. 3.
    How to make a sex chromosome · 2016
    No notice
  4. 4.

    Charlesworth D. Young sex chromosomes in plants and animals. New Phytol. 2019;224:1095-1107.

    Not in our library10.1111/nph.16002

  5. 5.

    Vicoso B. Molecular and evolutionary dynamics of animal sex-chromosome turnover. Nat Ecol Evol. 2019;3:1632-1641.

    Not in our library10.1038/s41559-019-1050-8

  6. 6.

    Griffin DK. Is the Y chromosome disappearing?—both sides of the argument. Chromosom Res. 2012;20:35-45.

    Not in our library10.1007/s10577-011-9252-1

  7. 7.

    Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, et al. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature. 2003;423:825-837.

    Not in our library10.1038/nature01722

  8. 8.

    Hughes JF, Skaletsky H, Pyntikova T, Graves TA, van Daalen SKM, Minx PJ, et al. Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature. 2010;463:536-539.

    Not in our library10.1038/nature08700

  9. 9.

    Hughes JF, Skaletsky H, Brown LG, Pyntikova T, Graves T, Fulton RS, et al. Strict evolutionary conservation followed rapid gene loss on human and rhesus Y chromosomes. Nature. 2012;483:82-86.

    Not in our library10.1038/nature10843

  10. 10.

    Bellott DW, Bellott DW, Hughes JF, Hughes JF, Skaletsky H, Skaletsky H, et al. Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators. Nature. 2014;508:494-499.

    Not in our library10.1038/nature13206

  11. 11.

    Soh YQS, Alföldi J, Pyntikova T, Brown LG, Graves T, Minx PJ, et al. Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes. Cell. 2014;159:800-813.

    Not in our library10.1016/j.cell.2014.09.052

  12. 12.

    Tomaszkiewicz M, Rangavittal S, Cechova M, Sanchez RC, Fescemyer HW, Harris R, et al. A time- and cost-effective strategy to sequence mammalian Y chromosomes: an application to the de novo assembly of gorilla Y. Genome Res. 2016;26:530-540.

    Not in our library10.1101/gr.199448.115

  13. 13.

    Bellott DW, Skaletsky H, Cho T-J, Brown L, Locke D, Chen N, et al. Avian W and mammalian Y chromosomes convergently retained dosage-sensitive regulators. Nat Genet. 2017;49:387-394.

    Not in our library10.1038/ng.3778

  14. 14.

    Mahajan S, Wei KH-C, Nalley MJ, Gibilisco L, Bachtrog D. De novo assembly of a young Drosophila Y chromosome using single-molecule sequencing and chromatin conformation capture. PLoS Biol. 2018;16:e2006348.

    Not in our library10.1371/journal.pbio.2006348

  15. 15.

    Hall AB, Papathanos P-A, Sharma A, Cheng C, Akbari OS, Assour L, et al. Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes. Proc National Acad Sci. 2016;113:E2114-E2123.

    Not in our library10.1073/pnas.1525164113

  16. 16.

    Zhou Q, Zhang J, Bachtrog D, An N, Huang Q, Jarvis ED, et al. Complex evolutionary trajectories of sex chromosomes across bird taxa. Science. 2014;346:1246338.

    Not in our library10.1126/science.1246338

  17. 17.

    Papadopulos AST, Chester M, Ridout K, Filatov DA. Rapid Y degeneration and dosage compensation in plant sex chromosomes. Proc National Acad Sci. 2015;112:13021-13026.

    Not in our library10.1073/pnas.1508454112

  18. 18.

    White MA, Kitano J, Peichel CL. Purifying selection maintains dosage-sensitive genes during degeneration of the threespine stickleback Y chromosome. Mol Biol Evol. 2015;32:1981-1995.

    Not in our library10.1093/molbev/msv078

  19. 19.

    Cortez D, Cortez D, Marin R, Marin R, Toledo-Flores D, Toledo-Flores D, et al. Origins and functional evolution of Y chromosomes across mammals. Nature. 2014;508:488-493.

    Not in our library10.1038/nature13151

  20. 20.

    Murphy WJ, Wilkerson AJP, Raudsepp T, Agarwala R, Schäffer AA, Stanyon R, et al. Novel gene acquisition on carnivore Y chromosomes. PLoS Genet. 2006;2:e43.

    Not in our library10.1371/journal.pgen.0020043

  21. 21.
    A gene catalogue of the euchromatic male-specific region of the horse Y chromosome: comparison with human and other mammals. · 2011
    Not checked
  22. 22.

    Janečka JE, Davis BW, Ghosh S, Paria N, Das PJ, Orlando L, et al. Horse Y chromosome assembly displays unique evolutionary features and putative stallion fertility genes. Nat Commun. 2018;9:2945.

    Not in our library10.1038/s41467-018-05290-6

  23. 23.

    Ellison C, Bachtrog D. Recurrent gene co-amplification on Drosophila X and Y chromosomes. PLoS Genet. 2019;15:e1008251.

    Not in our library10.1371/journal.pgen.1008251

  24. 24.

    Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature. 2012;484:55-61.

    Not in our library10.1038/nature10944

  25. 25.

    Roesti M, Moser D, Berner D. Recombination in the threespine stickleback genome-patterns and consequences. Mol Ecol. 2013;22:3014-3027.

    Not in our library10.1111/mec.12322

  26. 26.

    Glazer AM, Killingbeck EE, Mitros T, Rokhsar DS, Miller CT. Genome assembly improvement and mapping convergently evolved skeletal traits in sticklebacks with genotyping-by-sequencing. G3. 2015;5:1463-1472.

    Not in our library10.1534/g3.115.017905

  27. 27.

    Peichel CL, Sullivan ST, Liachko I, White MA. Improvement of the threespine stickleback genome using a Hi-C-based proximity-guided assembly. J Hered. 2017;108:693-700.

    Not in our library10.1093/jhered/esx058

  28. 28.

    Bell MA, Stewart JD, Park PJ. The world’s oldest fossil threespine stickleback fish. Copeia. 2009;2:256-265.

    Not in our library

  29. 29.

    Kitano J, Ross JA, Mori S, Kume M, Jones FC, Chan YF, et al. A role for a neo-sex chromosome in stickleback speciation. Nature. 2009;461:1079-1083.

    Not in our library10.1038/nature08441

  30. 30.
    Turnover of Sex Chromosomes in the Stickleback Fishes (Gasterosteidae) · 2009
    No notice
  31. 31.

    Varadharajan S, Rastas P, Löytynoja A, Matschiner M, Calboli FCF, Guo B, et al. A high-quality assembly of the nine-spined stickleback (Pungitius pungitius) genome. Genome Biol Evol. 2019;11:3291–308.

    Not in our library10.1093/gbe/evz240

  32. 32.

    Ross JA, Peichel CL. Molecular cytogenetic evidence of rearrangements on the Y chromosome of the threespine stickleback fish. Genetics. 2008;179:2173-2182.

    Not in our library10.1534/genetics.108.088559

  33. 33.

    Dudchenko O, Batra SS, Omer AD, Nyquist SK, Hoeger M, Durand NC, et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science. 2017;356:92–5.

    Not in our library10.1126/science.aal3327

  34. 34.

    Cech JN, Peichel CL. Identification of the centromeric repeat in the threespine stickleback fish (Gasterosteus aculeatus). Chromosom Res. 2015;23:767–79.

    Not in our library10.1007/s10577-015-9495-3

  35. 35.

    Durand NC, Robinson JT, Shamim MS, Machol I, Mesirov JP, Lander ES, et al. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst. 2016;3:99-101.

    Not in our library10.1016/j.cels.2015.07.012

  36. 36.

    AIexandrov IA, Medvedev LI, Mashkova TD, Kisselev LL, Romanova LY, Yurov YB. Definition of a new alpha satellite suprachromosomal family characterized by monomeric organization. Nucleic Acids Res. 1993;21:2209-2215.

    Not in our library10.1093/nar/21.9.2209

  37. 37.

    McNulty SM, Sullivan BA. Alpha satellite DNA biology: finding function in the recesses of the genome. Chromosom Res. 2018;26:115-138.

    Not in our library10.1007/s10577-018-9582-3

  38. 38.
    Centromere Repeats: Hidden Gems of the Genome · 2019
    No notice
  39. 39.

    Charlesworth B. Model for evolution of Y chromosomes and dosage compensation. Proc National Acad Sci. 1978;75:5618-5622.

    Not in our library10.1073/pnas.75.11.5618

  40. 40.

    Rice WR. Genetic hitchhiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics. 1987;116:161-167.

    Not in our library10.1093/genetics/116.1.161

  41. 41.

    Firth HV, Richards SM, Bevan AP, Clayton S, Corpas M, Rajan D, et al. DECIPHER: database of chromosomal imbalance and phenotype in humans using Ensembl resources. Am J Hum Genetics. 2009;84:524-533.

    Not in our library10.1016/j.ajhg.2009.03.010

  42. 42.
    Characterising and Predicting Haploinsufficiency in the Human Genome · 2010
    No notice
  43. 43.

    Gvozdev VA, Kogan GL, Usakin LA. The Y chromosome as a target for acquired and amplified genetic material in evolution. BioEssays. 2005;27:1256-1262.

    Not in our library10.1002/bies.20321

  44. 44.

    Saxena R, Brown LG, Hawkins T, Alagappan RK, Skaletsky H, Reeve MP, et al. The DAZ gene cluster on the human Y chromosome arose from an autosomal gene that was transposed, repeatedly amplified and pruned. Nat Genet. 1996;14:292-299.

    Not in our library10.1038/ng1196-292

  45. 45.

    Lahn BT, Page DC. Retroposition of autosomal mRNA yielded testis-specific gene family on human Y chromosome. Nat Genet. 1999;21:429-433.

    Not in our library10.1038/7771

  46. 46.

    Carvalho AB, Dobo BA, Vibranovski MD, Clark AG. Identification of five new genes on the Y chromosome of Drosophila melanogaster. Proc National Acad Sci. 2001;98:13225-13230.

    Not in our library10.1073/pnas.231484998

  47. 47.

    Mahajan S, Bachtrog D. Convergent evolution of Y chromosome gene content in flies. Nat Commun. 2017;8:785.

    Not in our library10.1038/s41467-017-00653-x

  48. 48.

    Tobler R, Nolte V, Schlötterer C. High rate of translocation-based gene birth on the Drosophila Y chromosome. Proc National Acad Sci. 2017;114:11721-11726.

    Not in our library10.1073/pnas.1706502114

  49. 49.
    Heterochromatin-Enriched Assemblies Reveal the Sequence and Organization of the Drosophila melanogaster Y Chromosome · 2018
    No notice
  50. 50.

    Cantarel BL, Cantarel BL, Korf I, Korf I, Robb SMC, Robb SMC, et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 2008;18:188-196.

    Not in our library10.1101/gr.6743907

  51. 51.
    MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects · 2011
    No notice
  52. 52.

    Long M, VanKuren NW, Chen S, Vibranovski MD. New gene evolution: little did we know. Annu Rev Genet. 2013;47:307-333.

    Not in our library10.1146/annurev-genet-111212-133301

  53. 53.

    Li G, Davis BW, Raudsepp T, Wilkerson AJP, Mason VC, Ferguson-Smith M, et al. Comparative analysis of mammalian Y chromosomes illuminates ancestral structure and lineage-specific evolution. Genome Res. 2013;23:1486-1495.

    Not in our library10.1101/gr.154286.112

  54. 54.

    Skinner BM, Sargent CA, Churcher C, Hunt T, Herrero J, Loveland JE, et al. The pig X and Y chromosomes: structure, sequence, and evolution. Genome Res. 2015;26:130-139.

    Not in our library10.1101/gr.188839.114

  55. 55.

    Brashear WA, Raudsepp T, Murphy WJ. Evolutionary conservation of Y chromosome ampliconic gene families despite extensive structural variation. Genome Res. 2018;28:1841-1851.

    Not in our library10.1101/gr.237586.118

  56. 56.

    Capel B. Vertebrate sex determination: evolutionary plasticity of a fundamental switch. Nat Rev Genet. 2017;18:675-689.

    Not in our library10.1038/nrg.2017.60

  57. 57.

    Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T, et al. A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proc National Acad Sci. 2012;109:2955-2959.

    Not in our library10.1073/pnas.1018392109

  58. 58.
    A Tandem Duplicate of Anti-Müllerian Hormone with a Missense SNP on the Y Chromosome Is Essential for Male Sex Determination in Nile Tilapia, Oreochromis niloticus · 2015
    No notice
  59. 59.
    Identification of the master sex determining gene in Northern pike (Esox lucius) reveals restricted sex chromosome differentiation · 2019
    No notice
  60. 60.
    A Trans-Species Missense SNP in Amhr2 Is Associated with Sex Determination in the Tiger Pufferfish, Takifugu rubripes (Fugu) · 2012
    No notice
  61. 61.

    Swarup H. Stages in the development of the stickleback Gasterosteus aculeatus (L.). J Embryol Exp Morph. 1958;6:373–83.

    Not in our library

  62. 62.

    Lewis ZR, McClellan MC, Postlethwait JH, Cresko WA, Kaplan RH. Female-specific increase in primordial germ cells marks sex differentiation in threespine stickleback (Gasterosteus aculeatus). J Morphol. 2008;269:909–21.

    Not in our library10.1002/jmor.10608

  63. 63.

    Sayres MAW, Lohmueller KE, Nielsen R. Natural selection reduced diversity on human Y chromosomes. PLoS Genet. 2014;10:e1004064.

    Not in our library10.1371/journal.pgen.1004064

  64. 64.

    Sayres MAW. Genetic diversity on the sex chromosomes. Genome Biol Evol. 2018;10:1064-1078.

    Not in our library10.1093/gbe/evy039

  65. 65.

    Hough J, Wang W, Barrett SCH, Wright SI. Hill-Robertson interference reduces genetic diversity on a young plant Y-chromosome. Genetics. 2017;207:685–695.

    Not in our library10.1534/genetics.117.300142

  66. 66.

    Bachtrog D, Charlesworth B. Reduced levels of microsatellite variability on the neo-Y chromosome of Drosophila miranda. Curr Biol. 2000;10:1025–31.

    Not in our library10.1016/s0960-9822(00)00656-4

  67. 67.

    Herrig DK, Modrick AJ, Brud E, Llopart A. Introgression in the Drosophila subobscura—D. madeirensis sister species: evidence of gene flow in nuclear genes despite mitochondrial differentiation. Evolution. 2014;68:705–19.

    Not in our library10.1111/evo.12295

  68. 68.

    Larracuente AM, Clark AG. Surprising differences in the variability of Y chromosomes in African and cosmopolitan populations of Drosophila melanogaster. Genetics. 2012;193:201–14.

    Not in our library10.1534/genetics.112.146167

  69. 69.

    Yi S, Charlesworth B. Contrasting patterns of molecular evolution of the genes on the new and old sex chromosomes of Drosophila miranda. Mol Biol Evol. 2000;17:703–17.

    Not in our library10.1093/oxfordjournals.molbev.a026349

  70. 70.

    Guo B, Chain FJ, Bornberg-Bauer E, Leder EH, Merilä J. Genomic divergence between nine- and three-spined sticklebacks. BMC Genomics. 2013;14:756.

    Not in our library10.1186/1471-2164-14-756

  71. 71.
    Linear assembly of a human centromere on the Y chromosome · 2018
    No notice
  72. 72.

    Bracewell R, Chatla K, Nalley MJ, Bachtrog D. Dynamic turnover of centromeres drives karyotype evolution in Drosophila. eLife. 2019;8:e49002.

    Not in our library10.7554/elife.49002

  73. 73.

    Henikoff S, Ahmad K, Malik HS. The centromere paradox: stable inheritance with rapidly evolving DNA. Science. 2001;293:1098-1102.

    Not in our library10.1126/science.1062939

  74. 74.

    Malik HS, Henikoff S. Conflict begets complexity: the evolution of centromeres. Curr Opin Genet Dev. 2002;12:711-718.

    Not in our library10.1016/s0959-437x(02)00351-9

  75. 75.

    Alkan CC, Cardone MFM, Catacchio CRC, Antonacci FF, O’Brien SJS, Ryder OAO, et al. Genome-wide characterization of centromeric satellites from multiple mammalian genomes. Genome Res. 2011;21:137-145.

    Not in our library10.1101/gr.111278.110

  76. 76.
    Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution · 2013
    No notice
  77. 77.

    Manuelidis L. Chromosomal localization of complex and simple repeated human DNAs. Chromosoma. 1978;66:23-32.

    Not in our library10.1007/bf00285813

  78. 78.

    Willard HF. Chromosome-specific organization of human alpha satellite DNA. Am J Hum Genet. 1985;37:524-532.

    Not in our library

  79. 79.

    Wolfe J, Darling SM, Erickson RP, Craig IW, Buckle VJ, Rigby PWJ, et al. Isolation and characterization of an alphoid centromeric repeat family from the human Y chromosome. J Mol Biol. 1985;182:477-485.

    Not in our library10.1016/0022-2836(85)90234-7

  80. 80.

    Pertile MD, Graham AN, Choo KHA, Kalitsis P. Rapid evolution of mouse Y centromere repeat DNA belies recent sequence stability. Genome Res. 2009;19:2202-2213.

    Not in our library10.1101/gr.092080.109

  81. 81.

    Miga KH, Newton Y, Jain M, Altemose N, Willard HF, Kent WJ. Centromere reference models for human chromosomes X and Y satellite arrays. Genome Res. 2014;24:697-707.

    Not in our library10.1101/gr.159624.113

  82. 82.

    Cech JN, Peichel CL. Centromere inactivation on a neo-Y fusion chromosome in threespine stickleback fish. Chromosom Res. 2016;24:437-450.

    Not in our library10.1007/s10577-016-9535-7

  83. 83.

    Crowson D, Barrett SCH, Wright SI. Purifying and positive selection influence patterns of gene loss and gene expression in the evolution of a plant sex chromosome system. Mol Biol Evol. 2017;34:1140-1154.

    Not in our library10.1093/molbev/msx064

  84. 84.

    Muyle A, Shearn R, Marais G. The evolution of sex chromosomes and dosage compensation in plants. Genome Biol Evol. 2017;9:627-645.

    Not in our library10.1093/gbe/evw282

  85. 85.

    Zhou Q, Bachtrog D. Sex-specific adaptation drives early sex chromosome evolution in Drosophila. Science. 2012;337:341-345.

    Not in our library10.1126/science.1225385

  86. 86.

    Hughes JF, Rozen S. Genomics and genetics of human and primate y chromosomes. Genom Hum Genetics. 2012;13:83-108.

    Not in our library10.1146/annurev-genom-090711-163855

  87. 87.

    Chibalina MV, Filatov DA. Plant Y chromosome degeneration is retarded by haploid purifying selection. Curr Biol. 2011;21:1475-1479.

    Not in our library10.1016/j.cub.2011.07.045

  88. 88.

    Rozen S, Skaletsky H, Marszalek JD, Minx PJ, Cordum HS, Waterston RH, et al. Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature. 2003;423:873-876.

    Not in our library10.1038/nature01723

  89. 89.

    Backström N, Ceplitis H, Berlin S, Ellegren H. Gene conversion drives the evolution of HINTW, an ampliconic gene on the female-specific avian W chromosome. Mol Biol Evol. 2005;22:1992-1999.

    Not in our library10.1093/molbev/msi198

  90. 90.

    Bhowmick BK, Satta Y, Takahata N. The origin and evolution of human ampliconic gene families and ampliconic structure. Genome Res. 2007;17:441-450.

    Not in our library10.1101/gr.5734907

  91. 91.

    Connallon T, Clark AG. Gene duplication, gene conversion and the evolution of the Y chromosome. Genetics. 2010;186:277-286.

    Not in our library10.1534/genetics.110.116756

  92. 92.

    Program NCS, Davis JK, Thomas PJ, Thomas JW. A W-linked palindrome and gene conversion in New World sparrows and blackbirds. Chromosom Res. 2010;18:543-553.

    Not in our library10.1007/s10577-010-9134-y

  93. 93.

    Marais GAB, Marais GAB, Campos PRA, Campos PRA, Gordo I, Gordo I. Can intra-Y gene conversion oppose the degeneration of the human Y chromosome? A simulation study. Genome Biol Evol. 2010;2:347-357.

    Not in our library10.1093/gbe/evq026

  94. 94.

    Hallast P, Balaresque P, Bowden GR, Ballereau S, Jobling MA. Recombination dynamics of a human Y-chromosomal palindrome: rapid GC-biased gene conversion, multi-kilobase conversion tracts, and rare inversions. PLoS Genet. 2013;9:e1003666.

    Not in our library10.1371/journal.pgen.1003666

  95. 95.

    Peneder P, Wallner B, Vogl C. Exchange of genetic information between therian X and Y chromosome gametologs in old evolutionary strata. Ecol Evol. 2017;7:8478-8487.

    Not in our library10.1002/ece3.3278

  96. 96.

    Trombetta B, Cruciani F. Y chromosome palindromes and gene conversion. Hum Genet. 2017;136:605-619.

    Not in our library10.1007/s00439-017-1777-8

  97. 97.

    Carvalho AB, Lazzaro BP, Clark AG. Y chromosomal fertility factors kl-2 and kl-3 of Drosophila melanogaster encode dynein heavy chain polypeptides. Proc National Acad Sci. 2000;97:13239–44.

    Not in our library10.1073/pnas.230438397

  98. 98.

    Zhang YE, Vibranovski MD, Krinsky BH, Long M. Age-dependent chromosomal distribution of male-biased genes in Drosophila. Genome Res. 2010;20:1526-1533.

    Not in our library10.1101/gr.107334.110

  99. 99.
    Chromosomal Redistribution of Male-Biased Genes in Mammalian Evolution with Two Bursts of Gene Gain on the X Chromosome · 2010
    No notice
  100. 100.

    Moens PB, Chen DJ, Shen Z, Kolas N, Tarsounas M, Heng HH, et al. Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosoma. 1997;106:207-215.

    Not in our library10.1007/s004120050241

  101. 101.

    Lange J, Yamada S, Tischfield SE, Pan J, Kim S, Zhu X, et al. The landscape of mouse meiotic double-strand break formation, processing, and repair. Cell. 2016;167:695-708.

    Not in our library10.1016/j.cell.2016.09.035

  102. 102.

    Sasaki M, Lange J, Keeney S. Genome destabilization by homologous recombination in the germ line. Nat Rev Mol Cell Bio. 2010;11:182-195.

    Not in our library10.1038/nrm2849

  103. 103.
    Canu: scalable and accurate long-read assembly via adaptive k -mer weighting and repeat separation · 2017
    No notice
  104. 104.
    Versatile and open software for comparing large genomes · 2004
    No notice
  105. 105.

    Durand NC, Shamim MS, Machol I, Rao SSP, Huntley MH, Lander ES, et al. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 2016;3:95-98.

    Not in our library10.1016/j.cels.2016.07.002

  106. 106.

    Kingsley DM, Zhu B, Osoegawa K, Jong PJD, Schein J, Marra M, et al. New genomic tools for molecular studies of evolutionary change in threespine sticklebacks. Behaviour. 2004;141:1331-1344.

    Not in our library

  107. 107.

    Peichel CL, Ross JA, Matson CK, Dickson M, Grimwood J, Schmutz J, et al. The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Curr Biol. 2004;14:1416-1424.

    Not in our library10.1016/j.cub.2004.08.030

  108. 108.

    Kingsley DM, Peichel CL. The molecular genetics of evolutionary change in sticklebacks. In: Östlund-Nilsson S, Mayer I, Huntingford F, editors. Boca Raton: CRC Press; 2006. p. 41–81.

    Not in our library

  109. 109.

    Urton JR, McCann SR, Peichel CL. Karyotype differentiation between two stickleback species (Gasterosteidae). Cytogenet Genome Res. 2011;135:150-159.

    Not in our library10.1159/000331232

  110. 110.

    Ferris P, Olson BJSC, Hoff PLD, Douglass S, Casero D, Prochnik S, et al. Evolution of an expanded sex-determining locus in Volvox. Science. 2010;328:351-354.

    Not in our library10.1126/science.1186222

  111. 111.

    Ewing B, Hillier L, Wendl MC, Green P. Base-calling of automated sequencer traces using Phred. I Accuracy assessment. Genome Res. 1998;8:175-185.

    Not in our library10.1101/gr.8.3.175

  112. 112.

    Ewing B, Green P. Base-calling of automated sequencer traces using Phred. II Error probabilities. Genome Res. 1998;8:186-194.

    Not in our library

  113. 113.

    Gordon D, Abajian C, Green P. Consed: a graphical tool for sequence finishing. Genome Res. 1998;8:195-202.

    Not in our library10.1101/gr.8.3.195

  114. 114.

    Shanfelter AF, Archambeault SL, White MA. Divergent fine-scale recombination landscapes between a freshwater and marine population of threespine stickleback fish. Genome Biol Evol. 2019;11:1573–85.

    Not in our library10.1093/gbe/evz101

  115. 115.
    Trimmomatic: a flexible trimmer for Illumina sequence data · 2014
    No notice
  116. 116.

    Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357-359.

    Not in our library10.1038/nmeth.1923

  117. 117.

    Broad Institute. Picard Tools. 2020; Available from: http://broadinstitute.github.io/picard Accessed 1 May 2020.

    Not in our library

  118. 118.

    Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841-842.

    Not in our library10.1093/bioinformatics/btq033

  119. 119.

    der Auwera GAV, Carneiro MO, Hartl C, Poplin R, del Angel G, Levy-Moonshine A, et al. From FastQ data to high-confidence variant calls: the genome analysis toolkit best practices pipeline. Curr Protoc Bioinform. 2013;43:11.10.1-11.10.33.

    Not in our library10.1002/0471250953.bi1110s43

  120. 120.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403-410.

    Not in our library10.1016/s0022-2836(05)80360-2

  121. 121.
    Automated generation of heuristics for biological sequence comparison · 2005
    No notice
  122. 122.

    Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24:1586-1591.

    Not in our library10.1093/molbev/msm088

  123. 123.

    Sardell JM, Cheng C, Dagilis AJ, Ishikawa A, Kitano J, Peichel CL, et al. Sex differences in recombination in sticklebacks. G3. 2018;8:1971-1983.

    Not in our library10.1534/g3.118.200166

  124. 124.

    Korf I. Gene finding in novel genomes. BMC Bioinformatics. 2004;5:59.

    Not in our library10.1186/1471-2105-5-59

  125. 125.
    AUGUSTUS at EGASP: using EST, protein and genomic alignments for improved gene prediction in the human genome · 2006
    No notice
  126. 126.
    TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions · 2013
    No notice
  127. 127.

    Roberts A, Pimentel H, Trapnell C, Pachter L. Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics. 2011;27:2325-2329.

    Not in our library10.1093/bioinformatics/btr355

  128. 128.

    Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210-3212.

    Not in our library10.1093/bioinformatics/btv351

  129. 129.
    BUSCO Applications from Quality Assessments to Gene Prediction and Phylogenomics · 2017
    No notice
  130. 130.
    HTSeq—a Python framework to work with high-throughput sequencing data · 2014
    No notice
  131. 131.

    Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of gene expression data. Bioinformatics. 2010;26:139-140.

    Not in our library10.1093/bioinformatics/btp616

  132. 132.

    Smit A, Hubley R. RepeatModeler Open-1.0. 2008; Available from: http://www.repeatmasker.org. Accessed 1 May 2020.

    Not in our library

  133. 133.

    Smit A, Hubley R, Green P. RepeatMasker Open-4.0. 2013; Available from: http://www.repeatmasker.org. Accessed 1 May 2020.

    Not in our library

  134. 134.

    Geneious Prime. 2019; Available from: https://www.geneious.com. Accessed 1 May 2020.

    Not in our library

  135. 135.

    Peichel CL, McCann SR, Ross JA, Naftaly AFS, Urton JR, Cech JN, et al. Threespine stickleback Y chromosome sequencing. Datasets. Sequence Read Archive. https://www.ncbi.nlm.nih.gov/bioproject/PRJNA591630. Accessed 27 June 2020.

    Not in our library

  136. 136.

    University of British Columbia. Whole genome sequencing of Paxton lake limnetic stickleback. Datasets. Sequence Read Archive. 2018. https://www.ncbi.nlm.nih.gov/sra/SRR5626528. Accessed 27 June 2020.

    Not in our library

  137. 137.

    University of British Columbia. Whole genome sequencing of Paxton lake benthic stickleback. Datasets. Sequence Read Archive. 2018. https://www.ncbi.nlm.nih.gov/sra/SRR5626529. Accessed 27 June 2020.

    Not in our library

  138. 138.

    Peichel CL, McCann SR, Ross JA, Naftaly AFS, Urton JR, Cech JN, et al. 2020; Available from: https://github.com/mikewhitelab/Y_Chromosome_Assembly Accessed 27 June 2020.

    Not in our library

  139. 139.

    Peichel CL, McCann SR, Ross JA, Naftaly AFS, Urton JR, Cech JN, et al. 2020. Available from: https://stickleback.genetics.uga.edu. Accessed 27 June 2020.

    Not in our library

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