Sex-dependent dominance maintains migration supergene in rainbow trout

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Abstract

Males and females often differ in their fitness optima for shared traits that have a shared genetic basis, leading to sexual conflict. Morphologically differentiated sex chromosomes can resolve this conflict and protect sexually antagonistic variation, but they accumulate deleterious mutations. However, how sexual conflict is resolved in species that lack differentiated sex chromosomes is largely unknown. Here we present a chromosome-anchored genome assembly for rainbow trout (Oncorhynchus mykiss) and characterize a 55-Mb double-inversion supergene that mediates sex-specific migratory tendency through sex-dependent dominance reversal, an alternative mechanism for resolving sexual conflict. The double inversion contains key photosensory, circadian rhythm, adiposity and sex-related genes and displays a latitudinal frequency cline, indicating environmentally dependent selection. Our results show sex-dependent dominance reversal across a large autosomal supergene, a mechanism for sexual conflict resolution capable of protecting sexually antagonistic variation while avoiding the homozygous lethality and deleterious mutations associated with typical heteromorphic sex chromosomes.

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Fig. 1: The duplicated rainbow trout genome.
Fig. 2: Divergence among karyotypes and linkage mapping suggest a double inversion, which exhibits latitudinal variation in frequency.
Fig. 3: Sex-dependent dominance of Omy05 genotypes.
Fig. 4: Restricted sex chromosome divergence and absence of sex-biased gene enrichment.
Fig. 5: Graphical hypothesis of O. mykiss life cycle.

photos taken by C. Phillis. Fish silhouettes provided by J. Moore, used with permission

Data availability

The reference genome assembly: GenBank Assembly Accession GCA_002163495.1, RefSeq Assembly Accession GCF_002163495.1. Raw sequence data used for the genome assembly: NCBI SRA Accession SRP086605 (Project ID: Project PRJNA335610). Raw sequence data used for whole-genome resequencing: NCBI SRA Accession SRP107028 (Project ID: PRJNA386519). New RNA-seq data generated for the genome annotation: NCBI SRA Accession SRP102416 (Project ID: PRJNA380337). Additional sequence data used for the NCBI RefSeq annotation are listed and described at https://www.ncbi.nlm.nih.gov/genome/annotation_euk/Oncorhynchus_mykiss/100/. Raw sequence data used for generating RAD SNP markers that were used for anchoring assembly scaffolds and contigs to chromosomes: USDA: NCBI SRA Accession SRP063932 (Project ID: PRJNA295850); UC Davis: NCBI SRA Accession SRP141092 (Project ID: PRJNA450873). NMFS data and analysis can be found at https://github.com/eriqande/Pearse_etal_NEE_NMFS_Data_Analysis.

References

  1. 1.

    Connallon, T. The geography of sex-specific selection, local adaptation, and sexual dimorphism. Evolution 69, 2333–2344 (2015).

  2. 2.

    Lande, R. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34, 292–305 (1980).

  3. 3.

    Mank, J. E. Population genetics of sexual conflict in the genomic era. Nat. Rev. Genet. 18, 721–730 (2017).

  4. 4.

    Barson, N. J. et al. Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature 528, 405–408 (2015).

  5. 5.

    Bachtrog, D. et al. Sex determination: why so many ways of doing it? PLoS Biol. 12, e1001899 (2014).

  6. 6.

    Rice, W. R. The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex chromosomes. Evolution 41, 911–914 (1987).

  7. 7.

    Fry, J. D. The genomic location of sexually antagonistic variation: some cautionary comments. Evolution 64, 1510–1516 (2010).

  8. 8.

    Cavoto, E., Neuenschwander, S., Goudet, J. & Perrin, N. Sex-antagonistic genes, XY recombination and feminized Y chromosomes. J. Evol. Biol. 31, 416–427 (2018).

  9. 9.

    Spencer, H. G. & Priest, N. K. The evolution of sex-specific dominance in response to sexually antagonistic selection. Am. Nat. 187, 658–666 (2016).

  10. 10.

    Grieshop, K. & Arnqvist, G. Sex-specific dominance reversal of genetic variation for fitness. PLoS Biol. 16, e2006810 (2018).

  11. 11.

    Küpper, C. et al. A supergene determines highly divergent male reproductive morphs in the ruff. Nat. Genet. 48, 79–83 (2016).

  12. 12.

    Lamichhaney, S. et al. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nat. Genet. 48, 84–88 (2016).

  13. 13.

    Tuttle, E. M. et al. Divergence and functional degradation of a sex chromosome-like supergene. Curr. Biol. 26, 344–350 (2016).

  14. 14.

    Wang, J. et al. A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493, 664–668 (2013).

  15. 15.

    Le Poul, Y. et al. Evolution of dominance mechanisms at a butterfly mimicry supergene. Nat. Commun. 5, 5644 (2014).

  16. 16.

    Llaurens, V., Whibley, A. & Joron, M. Genetic architecture and balancing selection: the life and death of differentiated variants. Mol. Ecol. 26, 2430–2448 (2017).

  17. 17.

    Blaser, O., Neuenschwander, S. & Perrin, N. Sex-chromosome turnovers: the hot-potato model. Am. Nat. 183, 140–146 (2013).

  18. 18.

    Lubieniecki, K. P. et al. Genomic instability of the sex-determining locus in Atlantic Salmon (Salmo salar). G3 (Bethesda) 5, 2513–2522 (2015).

  19. 19.

    Cavileer, T. D., Hunter, S. S., Olsen, J., Wenburg, J. & Nagler, J. J. A sex-determining gene (sdY) assay shows discordance between phenotypic and genotypic sex in wild populations of Chinook salmon. Trans. Am. Fish. Soc. 144, 423–430 (2015).

  20. 20.

    Eisbrenner, W. D. et al. Evidence for multiple sex-determining loci in Tasmanian Atlantic salmon (Salmo salar). Heredity (Edinb) 113, 86–92 (2014).

  21. 21.

    Perrin, N. Sex reversal: a fountain of youth for sex chromosomes? Evolution 63, 3043–3049 (2009).

  22. 22.

    Kendall, N. W. et al. Anadromy and residency in steelhead and rainbow trout (Oncorhynchus mykiss): a review of the processes and patterns. Can. J. Fish. Aquat. Sci. 72, 319–342 (2015).

  23. 23.

    Ohms, H. A., Sloat, M. R., Reeves, G. H., Jordan, C. E. & Dunham, J. B. Influence of sex, migration distance, and latitude on life history expression in steelhead and rainbow trout (Oncorhynchus mykiss). Can. J. Fish. Aquat. Sci. 71, 70–80 (2013).

  24. 24.

    Nichols, K. M., Edo, A. F., Wheeler, P. A. & Thorgaard, G. H. The genetic basis of smoltification-related traits in Oncorhynchus mykiss. Genetics 179, 1559–1575 (2008).

  25. 25.

    Pearse, D. E., Miller, M. R., Abadía-Cardoso, A. & Garza, J. C. Rapid parallel evolution of standing variation in a single, complex, genomic region is associated with life history in steelhead/rainbow trout. Proc. Biol. Sci. 281, 20140012 (2014).

  26. 26.

    Berthelot, C. et al. The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat. Commun. 5, 3657 (2014).

  27. 27.

    Lien, S. et al. The Atlantic salmon genome provides insights into rediploidization. Nature 533, 200–205 (2016).

  28. 28.

    Macqueen, D. J. & Johnston, I. A. A well-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification. Proc. Biol. Sci. 281, 20132881 (2014).

  29. 29.

    Hardie, D. C. & Hebert, P. D. The nucleotypic effects of cellular DNA content in cartilaginous and ray-finned fishes. Genome 46, 683–706 (2003).

  30. 30.

    Putnam, N. H. et al. Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Res. 26, 342–350 (2016).

  31. 31.

    Phillips, R. B. et al. Assignment of rainbow trout linkage groups to specific chromosomes. Genetics 174, 1661–1670 (2006).

  32. 32.

    Yano, A. et al. An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr. Biol. 22, 1423–1428 (2012).

  33. 33.

    Yano, A. et al. The sexually dimorphic on the Y-chromosome gene (sdY) is a conserved male‐specific Y‐chromosome sequence in many salmonids. Evol. Appl. 6, 486–496 (2013).

  34. 34.

    Roberts, R. B., Ser, J. R. & Kocher, T. D. Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science 326, 998–1001 (2009).

  35. 35.

    van Doorn, G. & Kirkpatrick, M. Turnover of sex chromosomes induced by sexual conflict. Nature 449, 909–912 (2007).

  36. 36.

    Vicoso, B., Kaiser, V. B. & Bachtrog, D. Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution. Proc. Natl Acad. Sci. USA 110, 6453–6458 (2013).

  37. 37.

    Kirkpatrick, M. & Guerrero, R. F. Signatures of sex-antagonistic selection on recombining sex chromosomes. Genetics 197, 531–541 (2014).

  38. 38.

    Phillips, R. B. et al. Characterization of the OmyY1 region on the rainbow trout Y chromosome. Int. J. Genomics 2013, 261730 (2013).

  39. 39.

    Phillips, R. B. et al. Recombination is suppressed over a large region of the rainbow trout Y chromosome. Anim. Genet. 40, 925–932 (2009).

  40. 40.

    Paigen, K. & Petkov, P. Mammalian recombination hot spots: properties, control and evolution. Nat. Rev. Genet. 11, 221–233 (2010).

  41. 41.

    Singer, A. et al. Sex-specific recombination rates in zebrafish (Danio rerio). Genetics 160, 649–657 (2002).

  42. 42.

    Sutherland, B. J. G. et al. Salmonid chromosome evolution as revealed by a novel method for comparing RADseq linkage maps. Genome Biol. Evol. 8, 3600–3617 (2016).

  43. 43.

    Blackmon, H. et al. Long-term fragility of Y chromosomes is dominated by short-term resolution of sexual antagonism. Genetics 207, 1621–1629 (2017).

  44. 44.

    Thompson, M. J. & Jiggins, C. D. Supergenes and their role in evolution. Heredity 113, 1–8 (2014).

  45. 45.

    Hale, M. C., McKinney, G. J., Thrower, F. P. & Nichols, K. M. RNA-seq reveals differential gene expression in the brains of juvenile resident and migratory smolt rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. Part D 20, 136–150 (2016).

  46. 46.

    Nakane, Y. et al. The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nat. Commun. 4, 2108 (2013).

  47. 47.

    Dickmeis, T. et al. Glucocorticoids play a key role in circadian cell cycle rhythms. PLoS Biol. 5, e78 (2007).

  48. 48.

    Vatine, G., Vallone, D., Gothilf, Y. & Foulkes, N. It’s time to swim! Zebrafish and the circadian clock. FEBS Lett. 585, 1485–1494 (2011).

  49. 49.

    Yoshitane, H. et al. JNK regulates the photic response of the mammalian circadian clock. EMBO Rep. 13, 455–461 (2012).

  50. 50.

    Kolodziejczak, M. et al. Serotonin modulates developmental microglia via 5-HT2B receptors: potential implication during synaptic refinement of retinogeniculate projections. ACS Chem. Neurosci. 6, 1219–1230 (2015).

  51. 51.

    Ori, M., De-Lucchini, S., Marras, G. & Nardi, I. Unraveling new roles for serotonin receptor 2B in development: key findings from Xenopus. Int. J. Dev. Biol. 57, 707–714 (2013).

  52. 52.

    Hecht, B. C., Campbell, N. R., Holecek, D. E. & Narum, S. R. Genome-wide association reveals genetic basis for the propensity to migrate in wild populations of rainbow and steelhead trout. Mol. Ecol. 22, 3061–3076 (2013).

  53. 53.

    Nichols, K. M. et al. Quantitative trait loci × maternal cytoplasmic environment interaction for development rate in Oncorhynchus mykiss. Genetics 175, 335–347 (2007).

  54. 54.

    Kunte, K. et al. doublesex is a mimicry supergene. Nature 507, 229–232 (2014).

  55. 55.

    Graf, M., Teo Qi-Wen, E.-R., Sarusie, M. V., Rajaei, F. & Winkler, C. Dmrt5 controls corticotrope and gonadotrope differentiation in the zebrafish pituitary. Mol. Endocrinol. 29, 187–199 (2015).

  56. 56.

    Guo, Y. et al. Molecular cloning, characterization, and expression in brain and gonad of Dmrt5 of zebrafish. Biochem. Biophys. Res. Commun. 324, 569–575 (2004).

  57. 57.

    Johnsen, H. & Andersen, Ø. Sex dimorphic expression of five dmrt genes identified in the Atlantic cod genome. The fish-specific dmrt2b diverged from dmrt2a before the fish whole-genome duplication. Gene 505, 221–232 (2012).

  58. 58.

    Xu, S., Xia, W., Zohar, Y. & Gui, J.-F. Zebrafish dmrta2 regulates the expression of cdkn2c in spermatogenesis in the adult testis. Biol. Reprod. 88, 1–12 (2013).

  59. 59.

    Aubin-Horth, N., Landry, C. R., Letcher, B. H. & Hofmann, H. A. Alternative life histories shape brain gene expression profiles in males of the same population. Proc. Biol. Sci. 272, 1655–1662 (2005).

  60. 60.

    Yin, J. et al. Genes and signaling networks regulated during zebrafish optic vesicle morphogenesis. BMC Genomics 15, 825 (2014).

  61. 61.

    Cimino, I. et al. Novel role for anti-Müllerian hormone in the regulation of GnRH neuron excitability and hormone secretion. Nat. Commun. 7, 10055 (2016).

  62. 62.

    Cavileer, T., Hunter, S., Okutsu, T., Yoshizaki, G. & Nagler, J. Identification of novel genes associated with molecular sex differentiation in the embryonic gonads of rainbow trout (Oncorhynchus mykiss). Sex. Dev. 3, 214–224 (2009).

  63. 63.

    von Hofsten, J. & Olsson, P.-E. Zebrafish sex determination and differentiation: involvement of FTZ-F1 genes. Reprod. Biol. Endocrinol. 3, 63 (2005).

  64. 64.

    Mrosek, N. et al. Transcriptional regulation of adipocyte formation by the liver receptor homologue 1 (Lrh1)-Small hetero-dimerization partner (Shp) network. Mol. Metab. 2, 314–323 (2013).

  65. 65.

    Hess, J. E., Zendt, J. S., Matala, A. R. & Narum, S. R. Genetic basis of adult migration timing in anadromous steelhead discovered through multivariate association testing. Proc. Biol. Sci. 283, 20153064 (2016).

  66. 66.

    Taranger, G. L. et al. Control of puberty in farmed fish. Gen. Comp. Endocrinol. 165, 483–515 (2010).

  67. 67.

    Kling, P. et al. The role of growth hormone in growth, lipid homeostasis, energy utilization and partitioning in rainbow trout: interactions with leptin, ghrelin and insulin-like growth factor I. Gen. Comp. Endocrinol. 175, 153–162 (2012).

  68. 68.

    Londraville, R. L., Prokop, J. W., Duff, R. J., Liu, Q. & Tuttle, M. On the molecular evolution of leptin, leptin receptor, and endospanin. Front. Endocrinol. (Lausanne) 8, 58 (2017).

  69. 69.

    Salmerón, C. et al. Effects of nutritional status on plasma leptin levels and in vitro regulation of adipocyte leptin expression and secretion in rainbow trout. Gen. Comp. Endocrinol. 210, 114–123 (2015).

  70. 70.

    Day, F. R. et al. Genomic analyses identify hundreds of variants associated with age at menarche and support a role for puberty timing in cancer risk. Nat. Genet. 49, 834–841 (2017).

  71. 71.

    Talukder, A. H., Li, D.-Q., Manavathi, B. & Kumar, R. Serine 28 phosphorylation of NRIF3 confers its co-activator function for estrogen receptor-α transactivation. Oncogene 27, 5233–5242 (2008).

  72. 72.

    Li, D. et al. NRIF3 is a novel coactivator mediating functional specificity of nuclear hormone receptors. Mol. Cell. Biol. 19, 7191–7202 (1999).

  73. 73.

    Singh, A. P. & Nüsslein-Volhard, C. Zebrafish stripes as a model for vertebrate colour pattern formation. Curr. Biol. 25, R81–R92 (2015).

  74. 74.

    Miller, M. R. et al. A conserved haplotype controls parallel adaptation in geographically distant salmonid populations. Mol. Ecol. 21, 237–249 (2012).

  75. 75.

    Thrower, F. P., Hard, J. J. & Joyce, J. E. Genetic architecture of growth and early life-history transitions in anadromous and derived freshwater populations of steelhead. J. Fish Biol. 65, 286–307 (2004).

  76. 76.

    Quinn, T. P. & Myers, K. W. Anadromy and the marine migrations of Pacific salmon and trout: Rounsefell revisited. Rev. Fish Biol. Fish. 14, 421–442 (2004).

  77. 77.

    Czorlich, Y., Aykanat, T., Erkinaro, J., Orell, P. & Primmer, C. R. Rapid sex-specific evolution of age at maturity is shaped byo genetic architecture in Atlantic salmon. Nat. Ecol. Evol. 2, 1800–1807 (2018).

  78. 78.

    Patten, M. M., Haig, D. & Ubeda, F. Fitness variation due to sexual antagonism and linkage disequilibrium. Evolution 64, 3638–3642 (2010).

  79. 79.

    Connallon, T. & Clark, A. G. Balancing selection in species with separate sexes: insights from Fisher’s geometric model. Genetics 197, 991–1006 (2014).

  80. 80.

    Kardos, M. & Shafer, A. B. A. The peril of gene-targeted conservation. Trends Ecol. Evol. 33, 827–839 (2018).

  81. 81.

    Pearse, D. E. Saving the spandrels? Adaptive genomic variation in conservation and fisheries management. J. Fish Biol. 89, 2697–2716 (2016).

  82. 82.

    Hirsch, C. N. et al. Draft assembly of elite inbred line PH207 provides insights into genomic and transcriptome diversity in maize. Plant Cell 28, 2700–2714 (2016).

  83. 83.

    Rastas, P., Paulin, L., Hanski, I., Lehtonen, R. & Auvinen, P. Lep-MAP: fast and accurate linkage map construction for large SNP datasets. Bioinformatics 29, 3128–3134 (2013).

  84. 84.

    Palti, Y. et al. The development and characterization of a 57K single nucleotide polymorphism array for rainbow trout. Mol. Ecol. Resour. 15, 662–672 (2015).

  85. 85.

    Harris, R. S. Improved Pairwise Alignment of Genomic DNA. PhD thesis, Pennsylvania State Univ. (2007).

  86. 86.

    Krzywinski, M. I. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639–1645 (2009).

  87. 87.

    Gao, G. et al. A new single nucleotide polymorphism database for rainbow trout generated through whole genome resequencing. Front. Genet. 9, 147 (2018).

  88. 88.

    Emms, D. M. & Kelly, S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16, 157 (2015).

  89. 89.

    Garrison, E. & Marth, G. Haplotype-based variant detection from short-read sequencing. Preprint at https://arxiv.org/pdf/1207.3907.pdf (2012).

  90. 90.

    Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

  91. 91.

    Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552 (2000).

  92. 92.

    Drummond, A. J. & Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007).

  93. 93.

    Chiang, C. et al. SpeedSeq: ultra-fast personal genome analysis and interpretation. Nat. Methods 12, 966–968 (2015).

  94. 94.

    Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/pdf/1303.3997.pdf (2013).

  95. 95.

    Pedersen, B. S. & Quinlan, A. Mosdepth: quick coverage calculation for genomes and exomes. Bioinformatics 34, 867–868 (2018).

  96. 96.

    Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527 (2016).

  97. 97.

    Kodama, M., Brieuc, M. S., Devlin, R. H., Hard, J. J. & Naish, K. A. Comparative mapping between Coho Salmon (Oncorhynchus kisutch) and three other salmonids suggests a role for chromosomal rearrangements in the retention of duplicated regions following a whole genome duplication event. G3 (Bethesda) 4, 1717–1730 (2014).

  98. 98.

    Brieuc, M. S., Waters, C. D., Seeb, J. E. & Naish, K. A. A dense linkage map for Chinook salmon (Oncorhynchus tshawytscha) reveals variable chromosomal divergence after an ancestral whole genome duplication event. G3 (Bethesda) 4, 447–460 (2014).

  99. 99.

    Waples, R. K., Seeb, L. W. & Seeb, J. E. Linkage mapping with paralogs exposes regions of residual tetrasomic inheritance in chum salmon (Oncorhynchus keta). Mol. Ecol. Resour. 16, 17–28 (2016).

  100. 100.

    Larson, W. A. et al. Identification of multiple QTL hotspots in sockeye salmon (Oncorhynchus nerka) using genotyping-by-sequencing and a dense linkage map. J. Hered. 107, 122–133 (2016).

  101. 101.

    Rundio, D. E., Williams, T. H., Pearse, D. E. & Lindley, S. T. Male-biased sex ratio of nonoanadromous Oncorhynchus mykiss in a partially migratory population in California. Ecol. Freshw. Fish 21, 293–299 (2012).

  102. 102.

    Abadía-Cardoso, A., Anderson, E. C., Pearse, D. E. & Garza, J. C. Large-scale parentage analysis reveals reproductive patterns and heritability of spawn timing in a hatchery population of steelhead (Oncorhynchus mykiss). Mol. Ecol. 22, 4733–4746 (2013).

  103. 103.

    Brunelli, J. P., Wertzler, K. J., Sundin, K. & Thorgaard, G. H. Y-specific sequences and polymorphisms in rainbow trout and Chinook salmon. Genome 51, 739–748 (2008).

  104. 104.

    Bond, M. H., Hayes, S. A., Hanson, C. V. & MacFarlane, R. B. Marine survival of steelhead (Oncorhynchus mykiss) enhanced by a seasonally closed estuary. Can. J. Fish. Aquat. Sci. 65, 2242–2252 (2008).

  105. 105.

    Jombart, T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008).

  106. 106.

    Hill, W. G. & Robertson, A. Linkage disequilibrium in finite populations. Theor. Appl. Genet. 38, 226–231 (1968).

  107. 107.

    Pritchard, J. K. & Przeworski, M. Linkage disequilibrium in humans: models and data. Am. J. Hum. Genet. 69, 1–14 (2001).

  108. 108.

    Warnes, G. & Leisch, F. The genetics Package: Population Genetics. R package version 1.2.0 (2005).

  109. 109.

    Kamvar, Z. N., Tabima, J. F. & Grünwald, N. J. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, e281 (2014).

  110. 110.

    Cavalli-Sforza, L. L. & Edwards, A. W. F. Phylogenetic analysis: models and estimation procedures. Evolution 21, 550–570 (1967).

  111. 111.

    Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425 (1987).

  112. 112.

    Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).

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Acknowledgements

We thank H. Fish, K. Pipal and many others for help with fieldwork; V. Apkenas, A. Carlo and E. Campbell for assistance with data collection and analysis; and M. Readdie and F. Aryas for support at the University of California Landels-Hill Big Creek Reserve. Samples and data for the geographic survey were provided by M. Ackerman, S. Lewis, S. Narum, K. Nichols, S. Northrup (Freshwater Fisheries Society of British Columbia), E. Taylor (University of British Columbia), D. Teel and K. Warheit. Compute Canada provided the computing resources used in repeat annotation and analysis. We thank R. Long and K. Shewbridge for their help in DNA sample preparation for sequencing and genotyping and in the preparation of RAD-seq libraries, and K. Martin and Troutlodge for the permission to use samples from their germplasm for genotyping. We also thank the Genomics Core at Washington State University, Spokane, the University of Idaho Genomics Core and the Vincent J. Coates Genomics Sequencing Laboratory at University of California, Berkeley for performing DNA library preparation and clonal lines’ resequencing. The genome resequencing of the Whale Rock female clonal line was conducted in collaboration with M. Garvin, Oregon State University. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. USDA is an equal opportunity provider and employer. This project was supported by funds from the USDA-ARS (in-house project nos. 1930-31000-009 and 8082-31000-012). DH clonal line resequencing was supported by an Agriculture and Food Research Initiative Competitive Grant (no. 2015-07185) from the USDA National Institute of Food and Agriculture and by an NRSP8 Aquaculture Genome funding seed grant to M.G. and G.T. The whole-genome resequencing data provided by K. Naish was obtained from a project supported by an Agriculture and Food Research Initiative Competitive Grant (no. 2012-67015-19960) from the USDA National Institute of Food and Agriculture. Funding for bioinformatics and statistical support at CIGENE (Norwegian University of Life Sciences) was provided by NFR grants (nos. 208481, 226266 and 275310). Bioinformatics analyses were performed using resources at the Orion Computing Cluster at CIGENE, with storage resources provided by the Norwegian National Infrastructure for Research Data (project no. NS9055K). We acknowledge the help of S. Karoliussen and M. Arnyasi at CIGENE for generating rainbow trout genotypes and M. Baranski for work on the genetic linkage maps. C. R. Primmer and K. Nichols provided valuable comments on the draft manuscript.

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S.Lien, Y.P. and A.G.H. co-conceived the genome assembly project. G.H.T. provided the Swanson clonal line for the reference genome. Y.P. and T.M. contributed SNP chip and RAD SNP genotype data for the linkage analysis. S.Lien and T.M. performed the linkage analyses. T.N. and S.Lien refined the assembly and built the chromosome sequences. K.B., G.B.-Z., D.S.-T. and O.B. designed and conducted the DeNovo MAGIC genome assembly of the Swanson clonal line Illumina sequence data. M.R.M. and L.C. provided RAD SNP data and linkage information for chromosome anchoring of the assembly scaffolds and contigs. D.E.P. and J.C.G. contributed the Dovetail sequence data for the genome assembly. G.G. incorporated the Dovetail sequence data for bridging and combing genome assembly scaffolds. S.Lien, Y.P., G.H.T., B.F.K., N.J.B. and D.E.P. designed the whole-genome resequencing study. G.H.T., B.F.K., S.Liu, K.K., K.A.N., M.S.O.B. and T.M. contributed samples, data and/or analysis to the resequencing study. D.R.M. and B.F.K. created and annotated the repeat library and performed the Tc1-mariner analysis. G.G. performed the bioinformatics analyses on the SNP chip genotype and RAD sequence data. N.J.B., G.G. and M.A.C. analysed the whole-genome resequencing data. S.Lien produced data and completed the comparative genomic analyses. N.J.B., M.K., T.N. and S.Lien produced and analysed the genotype data. M.M., M.K., T.N. and S.Lien made the draft nanopore genome assembly. N.J.B. and M.A.C. performed the population genomic analysis of the inversions using resequence data and analysed the gene content of the inversions. N.J.B. and T.N. performed the analysis of sex chromosome evolution. S.R.S., M.K. and T.N. generated RNA data. S.R.S. generated the orthogroup gene trees. N.J.B. and S.R.S. dated the inversions on Omy05. D.E.R., T.H.W., D.E.P., E.C.A., J.C.G. and S.T.L. conceived, designed and conducted the Omy05 capture–recapture field experiment, and D.E.R., E.C.A., D.E.P. and S.T.L. analysed the data. A.A.-C., J.C.G. and D.E.P. conceived, designed and conducted the SNP populations survey. E.B.R. and B.F.K. contributed additional data, and A.A.-C., E.C.A. and M.A.C. analysed the data. N.J.B., S.Lien, E.C.A., M.A.C., S.T.L., D.E.P. and B.F.K. created the figures. D.E.P., N.J.B., Y.P. and S.Lien wrote the paper with input from all authors. All authors read, commented on and approved the manuscript.

Correspondence to Devon E. Pearse or Yniv Palti or Sigbjørn Lien.

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Extended data

Extended Data Fig. 1 Activity periods, abundance, and historical proliferation of Tc1-Mariner families in Atlantic salmon, rainbow trout, and Chinook salmon.

a. Lower sequence similarity between family members indicates a more ancient family. Activity and abundance are generally consistent among the three species until the time corresponding to ~ 93% sequence similarity, after which substantial differences in activity have occurred in concert with salmonid lineage divergence. Tc1-Mariner families displayed were identified in Atlantic salmon and rainbow trout and occupied at least 0.1% of the genome in one of the three species. b. Stacked density plot of pairwise similarity between Tc1-Mariner family members. The large initial peak with a maxima at ~86% corresponds roughly to the same time that the salmonid-specific whole-genome duplication took place. In the time corresponding to more than 93% similarity, differences in activity begin to appear between Atlantic salmon and rainbow trout in accordance with their ancestral divergence (compare to Fig. 3a in Lien et al, 2016).

Extended Data Fig. 2 High-density linkage maps describing characteristic sex-specific recombination patterns and resolving variable chromosome numbers associated with centric fusions or fissions in rainbow trout.

a. Linkage map for the metacentric rainbow trout chromosome 8 (Omy08) demonstrating male recombination strongly localized towards both telomeres and female recombination repressed at the centromere. b. Linkage map for the metacentric rainbow trout chromosome 2 (Omy02) demonstrating elevated male recombination towards the telomeric region at the q-arm but repressed recombination at the p-arm typified by showing high sequence similarity to Omy03p. c. Linkage map for the acrocentric rainbow trout chromosome 29 (Omy29) with the sex-determining gene sdY located around 5 Mb demonstrating repressed male recombination for most of the chromosome except the telomeric region. d.-f. Rainbow trout chromosomes with variable chromosome numbers associated with centric fusions or fissions. Gaps in the linkage map at the centromere of Omy04, Omy14 and Omy25 are caused by fissions splitting metacentric chromosomes into two acrocentric chromosomes in some families.

Extended Data Fig. 3 Large polymorphic chromosomal rearrangements in the rainbow trout genome.

a. Ancestral (A) versus rearranged (R) chromosomal positions showing structure of inversion complexes on Omy05 and Omy20. b. Genetic linkage maps constructed for parents with alternate Omy05 and Omy20 haplotypes. Red line; female map for homozygous ancestral (AA) parents. Blue line; male map for homozygous ancestral (AA) parents. Orange line; female map for homozygous rearranged (RR) parents with marker order as in ancestral rearrangement. Green line; female map in heterozygous parents (AR).

Extended Data Fig. 4 Chromosomal rearrangements on rainbow trout chromosome 5 (Omy05) and conserved synteny with other salmonid species.

a. Ancestral (A) or rearranged (R) haplotypes on Omy05 characterized by two adjacent inversions of 22.83 and 32.94 Mb. B. Linkage map of recombination on chromosome Omy05 in males (green) and females (red). c.The alignment of Omy05 with the rest of the rainbow trout genome assembly show conserved collinear blocks of homeology with Omy12p, Omy29, Omy01p and Omy04p. d. The alignment of Omy05 with Atlantic salmon genome assembly (GCF_000233375.1) identifies highly conserved synteny with salmon chromosomes 1 and 10 (Ssa01qb and Ssa10qa). e. Alignment with the Arctic char genome (GCF_002910315.2) detects highly conserved synteny with char chromosomes 4 and 16 (Sal04 and Sal16). f. Alignment of Omy05 with coho salmon chromosome sequences (GCF_002021735.1) reveals conserved synteny with chromosomes 23 and 13 (Oki23 and Oki13). g. Comparison of Omy05 with RAD-based linkage maps for other Pacific salmon reveal a smaller fragment at centromere of Omy05 which is rearranged in coho, Chinook, chum and sockeye compared to rainbow trout, Arctic char and Atlantic salmon, and a larger rearrangement that differentiate coho and chinook from the other salmonid species.

Extended Data Fig. 5 Characterization of Omy05 double-inversion break points.

a. Contigs of the ancestral type spanning the three inversion break points on Omy05. The contigs were generated by long-read nanopore sequencing of a fish known to be homozygous for the ancestral configuration of the double inversion. b. Structure of the two variants of the double-inversion on Omy05 categorized as ancestral or rearranged. c. Scaffolds of the rearranged type spanning the three inversion break points on Omy05. The scaffolds were generated from the Swanson doubled haploid line known to be homozygous for the rearranged type of the double-inversion. Tables in the lower part of the figure list SNPs flanking the inversion break points, with positions in ancestral contigs or rearranged scaffolds, respectively, as well as boarders for the three break points in the ancestral type of the double-inversion.

Extended Data Fig. 6 Age estimates of the Omy05 inversion complex.

a. Age estimates from individual gene and CDS across the inversion showing lack of a strong pattern associated with inversion break points. b. Boxplot of age estimates for all CDS and genes that passed filtering, and the difference between the two estimates. Older estimates and wider confidence intervals are obtained from CDS than those based on gene sequences. c. Plot of the number of base differences between haplotypes for gene and CDS alignments and its effect on age estimation. Despite potentially having more variants because of the inclusion of introns, the gene alignments actually have fewer base differences per haplotype on average owing to the removal of poor quality intronic alignments by Gblocks. As a result, the CDS based alignments provide more informative alignments for dating the inversion complex. d. Estimate of inversion age in 10 Mb windows across the inversion complex for CDS estimates.

Extended Data Fig. 7 Full model results from antennae detection emigration model.

Full model results from antennae detection emigration model in Big Creek, showing mean (solid lines) and SD (dotted lines) of differential size-dependent migration of males and females with AR and AA, and RR Omy05 genotypes, with smoltification peaking at ~150 mm.

Extended Data Fig. 8 Linkage maps and conserved synteny with other salmonids for rainbow trout chromosome 29 (Omy29).

a. Sex-specific linkage maps for Omy29 (red dots; female, blue dots; male) show repressed recombination in males for the majority of Omy29. Genetic differentiation between males and females (Fst) is peaking at the sdY locus located at 5 Mb (yellow triangle) but is also elevated in the region between sdY and the centromere (Black Dot at 0 Mb). b. Regions of the rainbow trout genome homeologous with Omy29. Comparative genome sequence maps show highly conserved synteny with c. Atlantic salmon chromosome 11qb (ssa11qb) and d. Arctic char chromosome Sal05. e. Comparative mapping with coho salmon genome sequence reveals two larger rearrangements, one at 10 Mb and one at 30 Mb. f. Comparison of Omy29 with RAD-based linkage maps for other Pacific salmon show that the rearrangement at 10 Mb is conserved among coho, chinook, chum and sockeye and differentiated from rainbow trout and Atlantic salmon.

Extended Data Fig. 9 Genetic Diversity and Interrelationships of AA and RR Omy05 haplotypes.

Principal component (PC) analysis of genetic diversity estimated from (a) whole-genome sequence data genome-wide and, (b) within the chromosome Omy5 rearrangement. For both A and B, a random subset of 40,000 SNPs were examined from homozygous AA and RR individuals of known geographic origin and plotted with the principal components containing the most variance. Homozygous AA individuals are plotted as blue circles with homozygous RR individuals represented by red triangles, with numbers indicating geographic locations corresponding to Fig. 2d and Supplementary Information Table 4. While geographic structuring is apparent in the genome-wide SNP dataset, the inversion region separates clearly between RR and AA types with PC1 (28.76% of variation), and the subsequent second PC (7.49% of variation) corresponding to diversity within AA types. Similarly, population-level Neighbor-Joining trees of AA individuals and RR individuals from SNP survey data of homozygous AA individuals (c) and homozygous RR individuals (d) from sampled populations are depicted in a population level tree generated through chord distances. Support values for nodes with > 50% bootstrap support generated from 1,000 bootstrap replicates are indicated. Population numbers correspond to Fig. 2d and Supplementary Information Table 4.

Extended Data Fig. 10 Inversion Frequency as a Function of Mean Monthly Temperature.

For each month of the year below barrier North American populations of rainbow trout are plotted as mean monthly temperature (x – axis) and inversion frequency (y – axis). Points are sized proportionally to sample size (N). A weighted least squares regression is depicted with the adjusted R2 value for each month of the year.

Supplementary information

Supplementary Information

Supplementary Information and Tables 1–3, 5 and 8.

Reporting Summary

Supplementary Table 4

Details of all samples used.

Supplementary Table 6

Genes in the Omy05 inversion.

Supplementary Table 7

Homeologous blocks in the O. mykiss genome.

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Pearse, D.E., Barson, N.J., Nome, T. et al. Sex-dependent dominance maintains migration supergene in rainbow trout. Nat Ecol Evol 3, 1731–1742 (2019) doi:10.1038/s41559-019-1044-6

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