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Single-haplotype comparative genomics provides insights into lineage-specific structural variation during cat evolution

Nature Genetics volume 55, pages 1953–1963 (2023)Cite this article

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Abstract

The role of structurally dynamic genomic regions in speciation is poorly understood due to challenges inherent in diploid genome assembly. Here we reconstructed the evolutionary dynamics of structural variation in five cat species by phasing the genomes of three interspecies F1 hybrids to generate near-gapless single-haplotype assemblies. We discerned that cat genomes have a paucity of segmental duplications relative to great apes, explaining their remarkable karyotypic stability. X chromosomes were hotspots of structural variation, including enrichment with inversions in a large recombination desert with characteristics of a supergene. The X-linked macrosatellite DXZ4 evolves more rapidly than 99.5% of the genome clarifying its role in felid hybrid incompatibility. Resolved sensory gene repertoires revealed functional copy number changes associated with ecomorphological adaptations, sociality and domestication. This study highlights the value of gapless genomes to reveal structural mechanisms underpinning karyotypic evolution, reproductive isolation and ecological niche adaptation.

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Fig. 1: Assembly and synteny comparisons among the genomes of five cat species.
Fig. 2: Felid structural variation.
Fig. 3: DXZ4 evolution in placental mammals.
Fig. 4: Centromere annotation and evolution.
Fig. 5: ORG and V1R gene evolution in cats.

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Data availability

Assemblies are available in NCBI under accession numbers GCA_016509475.2, GCA_016509815.2, GCA_018350155.1, GCA_018350175.1, GCA_018350195.2 and GCA_018350215.1. OR gene sequences and DXZ4 alignments are found at: https://figshare.com/s/68266360874d5078bdf5.

Code availability

Publicly available software and packages were used in this study. No custom code was used. All software and packages used in this study are described within Methods section.

References

  1. Kronenberg, Z. N. et al. High-resolution comparative analysis of great ape genomes. Science 360, eaar6343 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Rhie, A. et al. Towards complete and error-free genome assemblies of all vertebrate species. Nature 592, 737–746 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Nurk, S. et al. The complete sequence of a human genome. Science 376, 44–53 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Miga, K. H. et al. Telomere-to-telomere assembly of a complete human X chromosome. Nature 585, 79–84 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Logsdon, G. A. et al. The structure, function and evolution of a complete human chromosome 8. Nature 593, 101–107 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Sedlazeck, F. J., Lee, H., Darby, C. A. & Schatz, M. C. Piercing the dark matter: bioinformatics of long-range sequencing and mapping. Nat. Rev. Genet. 19, 329–346 (2018).

    Article  CAS  PubMed  Google Scholar 

  7. Ahmad, S. F. et al. Dark matter of primate genomes: satellite DNA repeats and their evolutionary dynamics. Cells 9, 2714 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Johnson, W. E. et al. The late Miocene radiation of modern Felidae: a genetic assessment. Science 311, 73–77 (2006).

    Article  CAS  PubMed  Google Scholar 

  9. Li, G., Davis, B. W., Eizirik, E. & Murphy, W. J. Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae). Genome Res. 26, 1–11 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Li, G., Figueiró, H. V., Eizirik, E. & Murphy, W. J. Recombination-aware phylogenomics reveals the structured genomic landscape of hybridizing cat species. Mol. Biol. Evol. 36, 2111–2126 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Dobrynin, P. et al. Genomic legacy of the African cheetah, Acinonyx jubatus. Genome Biol. 16, 277 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Abascal, F. et al. Extreme genomic erosion after recurrent demographic bottlenecks in the highly endangered Iberian lynx. Genome Biol. 17, 251 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Johnson, W. E. et al. Genetic restoration of the Florida panther. Science 329, 1641–1645 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Montague, M. J. et al. Comparative analysis of the domestic cat genome reveals genetic signatures underlying feline biology and domestication. Proc. Natl Acad. Sci. USA 111, 17230–17235 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Koren, S. et al. De novo assembly of haplotype-resolved genomes with trio binning. Nat. Biotechnol. 36, 1174–1182 (2018).

    Article  CAS  Google Scholar 

  16. Cho, Y. S. et al. The tiger genome and comparative analysis with lion and snow leopard genomes. Nat. Commun. 4, 2433 (2013).

    Article  PubMed  Google Scholar 

  17. Buckley, R. M. et al. A new domestic cat genome assembly based on long sequence reads empowers feline genomic medicine and identifies a novel gene for dwarfism. PLoS Genet. 16, e1008926 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Bredemeyer, K. R., Harris, A. J., Li, G. & Zhao, L. Ultracontinuous single haplotype genome assemblies for the domestic cat (Felis catus) and Asian leopard cat (Prionailurus bengalensis). J. Hered. 197, 165–173 (2021).

    Article  Google Scholar 

  19. Meyne, J., Ratliff, R. L. & Moyzis, R. K. Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc. Natl Acad. Sci. USA 86, 7049–7053 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Peska, V. & Garcia, S. Origin, diversity, and evolution of telomere sequences in plants. Front. Plant Sci. 11, 117 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Fanning, T. G. Origin and evolution of a major feline satellite DNA. J. Mol. Biol. 197, 627–634 (1987).

    Article  CAS  PubMed  Google Scholar 

  22. Santos, S., Chaves, R. & Guedes-Pinto, H. Chromosomal localization of the major satellite DNA family (FA-SAT) in the domestic cat. Cytogenet. Genome Res. 107, 119–122 (2004).

    Article  CAS  PubMed  Google Scholar 

  23. Wurster-Hill, D. H. & Centerwall, W. R. The interrelationships of chromosome banding patterns in canids, mustelids, hyena, and felids. Cytogenet. Cell Genet. 34, 178–192 (1982).

    Article  CAS  PubMed  Google Scholar 

  24. Bailey, J. A., Baertsch, R., Kent, W. J., Haussler, D. & Eichler, E. E. Hotspots of mammalian chromosomal evolution. Genome Biol. 5, R23 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Marques-Bonet, T., Ryder, O. A. & Eichler, E. E. Sequencing primate genomes: what have we learned? Annu. Rev. Genomics Hum. Genet. 10, 355–386 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Cantsilieris, S. et al. An evolutionary driver of interspersed segmental duplications in primates. Genome Biol. 21, 202 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Mao, Y. et al. A high-quality bonobo genome refines the analysis of hominid evolution. Nature 594, 77–81 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Numanagic, I. et al. Fast characterization of segmental duplications in genome assemblies. Bioinformatics 34, i706–i714 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Vollger, M. R. et al. Segmental duplications and their variation in a complete human genome. Science 376, eabj6965 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Charlesworth, D. & Charlesworth, B. Sex chromosomes: evolution of the weird and wonderful. Curr. Biol. 15, R129–R131 (2005).

    Article  CAS  PubMed  Google Scholar 

  31. Larson, E. L., Keeble, S., Vanderpool, D., Dean, M. D. & Good, J. M. The composite regulatory basis of the large X-effect in mouse speciation. Mol. Biol. Evol. 34, 282–295 (2017).

    CAS  PubMed  Google Scholar 

  32. Charlesworth, B., Coyne, J. A. & Barton, N. H. The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 130, 113–146 (1987).

    Article  Google Scholar 

  33. Cheng, C. & Kirkpatrick, M. Inversions are bigger on the X chromosome. Mol. Ecol. 28, 1238–1245 (2019).

    Article  CAS  PubMed  Google Scholar 

  34. Figueiró, H. V. et al. Genome-wide signatures of complex introgression and adaptive evolution in the big cats. Sci. Adv. 3, e1700299 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Ferree, P. M. & Prasad, S. How can satellite DNA divergence cause reproductive isolation? Let us count the chromosomal ways. Genet. Res. Int. 2012, 430136 (2012).

    PubMed  PubMed Central  Google Scholar 

  36. Bayes, J. J. & Malik, H. S. Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 326, 1538–1541 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Bredemeyer, K. R. et al. Rapid macrosatellite evolution promotes X-linked hybrid male sterility in a Feline interspecies cross. Mol. Biol. Evol. 38, 5588–5609 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Figueroa, D. M., Darrow, E. M. & Chadwick, B. P. Two novel DXZ4-associated long noncoding RNAs show developmental changes in expression coincident with heterochromatin formation at the human (Homo sapiens) macrosatellite repeat. Chromosome Res. 23, 733–752 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Dossin, F. & Heard, E. The molecular and nuclear dynamics of X-chromosome inactivation. Cold Spring Harb. Perspect. Biol. 14, a040196 (2022).

    CAS  PubMed  Google Scholar 

  40. Bonora, G. et al. Orientation-dependent Dxz4 contacts shape the 3D structure of the inactive X chromosome. Nat. Commun. 9, 1445 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Vollger, M. R., Kerpedjiev, P., Phillippy, A. M. & Eichler, E. E. StainedGlass: interactive visualization of massive tandem repeat structures with identity heatmaps. Bioinformatics 38, 2049–2051 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Horakova, A. H. et al. The mouse DXZ4 homolog retains Ctcf binding and proximity to Pls3 despite substantial organizational differences compared to the primate macrosatellite. Genome Biol. 13, R70 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Froberg, J. E., Pinter, S. F., Kriz, A. J., Jégu, T. & Lee, J. T. Megadomains and superloops form dynamically but are dispensable for X-chromosome inactivation and gene escape. Nat. Commun. 9, 5004 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Brashear, W. A., Bredemeyer, K. R. & Murphy, W. J. Genomic architecture constrained placental mammal X chromosome evolution. Genome Res. 31, 1353–1365 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Andergassen, D. et al. In vivo Firre and Dxz4 deletion elucidates roles for autosomal gene regulation. eLife 8, e47214 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Abe, H. et al. Active DNA damage response signaling initiates and maintains meiotic sex chromosome inactivation. Nat. Commun. 13, 7212 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Abe, H. et al. The initiation of meiotic sex chromosome inactivation sequesters DNA damage signaling from autosomes in mouse spermatogenesis. Curr. Biol. 30, 408–420 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Altemose, N. et al. Complete genomic and epigenetic maps of human centromeres. Science 376, eabl4178 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Carbone, L. et al. Evolutionary movement of centromeres in horse, donkey, and zebra. Genomics 87, 777–782 (2006).

    Article  CAS  PubMed  Google Scholar 

  50. Raudsepp, T., Finno, C. J., Bellone, R. R. & Petersen, J. L. Ten years of the horse reference genome: insights into equine biology, domestication and population dynamics in the post-genome era. Anim. Genet. 50, 569–597 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Henikoff, S., Ahmad, K. & Malik, H. S. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293, 1098–1102 (2001).

    Article  CAS  PubMed  Google Scholar 

  52. Young, J. M. & Trask, B. J. The sense of smell: genomics of vertebrate odorant receptors. Hum. Mol. Genet. 11, 1153–1160 (2002).

    Article  CAS  PubMed  Google Scholar 

  53. Hayden, S. et al. Ecological adaptation determines functional mammalian olfactory subgenomes. Genome Res. 20, 1–9 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Hughes, G. M. et al. The birth and death of olfactory receptor gene families in mammalian niche adaptation. Mol. Biol. Evol. 35, 1390–1406 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Carroll, R. A. et al. A novel fishing cat reference genome for the evaluation of potential germline risk variants. Preprint at bioRxiv https://doi.org/10.1101/2022.11.17.516921 (2022).

  56. Sunquist, M. & Sunquist, F. Wild Cats of the World (Univ. Chicago Press, 2017).

  57. Nel, J. A. J. Handbook of the Mammals of the World, Vol. 1: Carnivores (Lynx Edicions, 2009).

  58. Dunkel, A. et al. Nature’s chemical signatures in human olfaction: a foodborne perspective for future biotechnology. Angew. Chem. Int. Ed. 53, 7124–7143 (2014).

    Article  CAS  Google Scholar 

  59. Moran, Y., Barzilai, M. G., Liebeskind, B. J. & Zakon, H. H. Evolution of voltage-gated ion channels at the emergence of Metazoa. J. Exp. Biol. 218, 515–525 (2015).

    Article  PubMed  Google Scholar 

  60. Nei, M. & Rooney, A. P. Concerted and birth-and-death evolution of multigene families. Annu. Rev. Genet. 39, 121–152 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Zhao, J., Teufel, A. I., Liberles, D. A. & Liu, L. A generalized birth and death process for modeling the fates of gene duplication. BMC Evol. Biol. 15, 275 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  62. Newman, T. & Trask, B. J. Complex evolution of 7E olfactory receptor genes in segmental duplications. Genome Res. 13, 781–793 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Niimura, Y., Matsui, A. & Touhara, K. Corrigendum: extreme expansion of the olfactory receptor gene repertoire in African elephants and evolutionary dynamics of orthologous gene groups in 13 placental mammals. Genome Res. 25, 926 (2015).

    PubMed  PubMed Central  Google Scholar 

  64. Soso, S. B. & Koziel, J. A. Characterizing the scent and chemical composition of Panthera leo marking fluid using solid-phase microextraction and multidimensional gas chromatography–mass spectrometry-olfactometry. Sci. Rep. 7, 5137 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  65. Nosil, P. & Feder, J. L. Genomic divergence during speciation: causes and consequences. Phil. Trans. R. Soc. B 367, 332–342 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  66. Miga, K. H. & Sullivan, B. A. Expanding studies of chromosome structure and function in the era of T2T genomics. Hum. Mol. Genet. 30, R198–R205 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Wold, J. et al. Expanding the conservation genomics toolbox: incorporating structural variants to enhance genomic studies for species of conservation concern. Mol. Ecol. 30, 5949–5965 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Formenti, G. et al. The era of reference genomes in conservation genomics. Trends Ecol. Evol. 37, 197–202 (2022).

    Article  CAS  PubMed  Google Scholar 

  69. Mérot, C., Oomen, R. A., Tigano, A. & Wellenreuther, M. A roadmap for understanding the evolutionary significance of structural genomic variation. Trends Ecol. Evol. 35, 561–572 (2020).

    Article  PubMed  Google Scholar 

  70. Lovell, J. T. et al. GENESPACE tracks regions of interest and gene copy number variation across multiple genomes. eLife 11, e78526 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  71. Li, G. et al. A high-resolution SNP array-based linkage map anchors a new domestic cat draft genome assembly and provides detailed patterns of recombination. G3 6, 1607–1616 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  72. Jégu, T., Aeby, E. & Lee, J. T. The X chromosome in space. Nat. Rev. Genet. 18, 377–389 (2017).

    Article  PubMed  Google Scholar 

  73. Menotti-Raymond, M. et al. A genetic linkage map of microsatellites in the domestic cat (Felis catus). Genomics 57, 9–23 (1999).

    Article  CAS  PubMed  Google Scholar 

  74. Menotti-Raymond, M. et al. Second-generation integrated genetic linkage/radiation hybrid maps of the domestic cat (Felis catus). J. Hered. 94, 95–106 (2003).

    Article  CAS  PubMed  Google Scholar 

  75. Miller, S. A., Dykes, D. D. & Polesky, H. F. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16, 1215 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Ramani, V. et al. Mapping 3D genome architecture through in situ DNase Hi-C. Nat. Protoc. 11, 2104–2121 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Andrews, S. FastQC. A quality control tool for high throughput sequence data. https://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (2010).

  78. Koren, S. et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 27, 722–736 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Hu, J., Fan, J., Sun, Z. & Liu, S. NextPolish: a fast and efficient genome polishing tool for long-read assembly. Bioinformatics 36, 2253–2255 (2020).

    Article  CAS  PubMed  Google Scholar 

  80. Mikheenko, A., Prjibelski, A., Saveliev, V., Antipov, D. & Gurevich, A. Versatile genome assembly evaluation with QUAST-LG. Bioinformatics 34, i142–i150 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).

    Article  PubMed  Google Scholar 

  82. Marçais, G. et al. MUMmer4: a fast and versatile genome alignment system. PLoS Comput. Biol. 14, e1005944 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  83. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Rice, E. S. et al. Continuous chromosome-scale haplotypes assembled from a single interspecies F1 hybrid of yak and cattle. Gigascience 9, giaa029 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  85. Ghurye, J., Pop, M., Koren, S., Bickhart, D. & Chin, C.-S. Scaffolding of long read assemblies using long range contact information. BMC Genomics 18, 527 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  86. Ghurye, J. et al. Integrating Hi-C links with assembly graphs for chromosome-scale assembly. PLoS Comput. Biol. 15, e1007273 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Dudchenko, O. et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science 356, 92–95 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Alonge, M. et al. RaGOO: fast and accurate reference-guided scaffolding of draft genomes. Genome Biol. 20, 224 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  89. Durand, N. C. et al. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 3, 95–98 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Robinson, J. T. et al. Juicebox.js provides a cloud-based visualization system for Hi-C data. Cell Syst. 6, 256–258 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Seibt, K. M., Schmidt, T. & Heitkam, T. FlexiDot: highly customizable, ambiguity-aware dotplots for visual sequence analyses. Bioinformatics 34, 3575–3577 (2018).

    Article  CAS  PubMed  Google Scholar 

  92. Horakova, A. H., Moseley, S. C., McLaughlin, C. R., Tremblay, D. C. & Chadwick, B. P. The macrosatellite DXZ4 mediates CTCF-dependent long-range intrachromosomal interactions on the human inactive X chromosome. Hum. Mol. Genet. 21, 4367–4377 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Chadwick, B. P. DXZ4 chromatin adopts an opposing conformation to that of the surrounding chromosome and acquires a novel inactive X-specific role involving CTCF and antisense transcripts. Genome Res. 18, 1259–1269 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis, v. 3.61. http://mesquiteproject.org (2019).

  96. Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Harris, A. J., Foley, N. M., Williams, T. L. & Murphy, W. J. Tree house explorer: a novel genome browser for phylogenomics. Mol. Biol. Evol. 39, msac130 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Murphy, W. J., Foley, N. M., Bredemeyer, K. R., Gatesy, J. & Springer, M. S. Phylogenomics and the genetic architecture of the placental mammal radiation. Annu. Rev. Anim. Biosci. 9, 29–53 (2021).

    Article  CAS  PubMed  Google Scholar 

  99. O’Brien, S. J., Graphodatsky, A. S. & Perelman, P. L. Atlas of Mammalian Chromosomes (John Wiley & Sons, 2020).

  100. Flynn, J. M. et al. RepeatModeler2 for automated genomic discovery of transposable element families. Proc. Natl Acad. Sci. USA 117, 9451–9457 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Vlahovic, I. et al. Global repeat map algorithm (GRM) reveals differences in α satellite number of tandem and higher order repeats (HORs) in human, Neanderthal and chimpanzee genomes—novel tandem repeat database. In Proc. 2020 43rd International Convention on Information, Communication and Electronic Technology (MIPRO) (IEEE, 2020).

  102. Olson, D. & Wheeler, T. ULTRA: a model based tool. detect tandem repeats. ACM BCB 2018, 37–46 (2018).

    PubMed  PubMed Central  Google Scholar 

  103. Davis, B. W. et al. A high-resolution cat radiation hybrid and integrated FISH mapping resource for phylogenomic studies across Felidae. Genomics 93, 299–304 (2009).

    Article  CAS  PubMed  Google Scholar 

  104. Kent, J. W. BLAT—the BLAST-like alignment tool. Genome Res. 12, 656–664 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Murphy, W. J. et al. A radiation hybrid map of the cat genome: implications for comparative mapping. Genome Res. 10, 691–702 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Erdman, C. bcp: a package for performing a Bayesian analysis of change point problems. R package version 1.8.4. https://www.rdocumentation.org/packages/bcp/versions/1.8.4 (2007).

  107. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    Article  CAS  PubMed  Google Scholar 

  108. Smit, A. F. A., Hubley, R. & Green, P. RepeatMasker Open-4.0. 2013–2015. http://www.repeatmasker.org (2015).

  109. Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).

    Article  CAS  PubMed  Google Scholar 

  111. Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  112. Chen, K., Durand, D. & Farach-Colton, M. NOTUNG: a program for dating gene duplications and optimizing gene family trees. J. Comput. Biol. 7, 429–447 (2000).

    Article  CAS  PubMed  Google Scholar 

  113. Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).

    Article  CAS  PubMed  Google Scholar 

  114. García-Alcalde, F. et al. Qualimap: evaluating next-generation sequencing alignment data. Bioinformatics 28, 2678–2679 (2012).

    Article  PubMed  Google Scholar 

  115. Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  116. Van der Auwera, G. A. et al. From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr. Protoc. Bioinformatics 43, 11.10.1–11.10.33 (2013).

    PubMed  Google Scholar 

  117. McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Adrion, J. R., Galloway, J. G. & Kern, A. D. Predicting the landscape of recombination using deep learning. Mol. Biol. Evol. 37, 1790–1808 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Kumar, S. & Subramanian, S. Mutation rates in mammalian genomes. Proc. Natl Acad. Sci. USA 99, 803–808 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Ebert, P. et al. Haplotype-resolved diverse human genomes and integrated analysis of structural variation. Science 372, eabf7117 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Ren, J. & Chaisson, M. J. P. lra: a long read aligner for sequences and contigs. PLoS Comput. Biol. 17, e1009078 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Vollger, M. R. et al. Long-read sequence and assembly of segmental duplications. Nat. Methods 16, 88–94 (2019).

    Article  CAS  PubMed  Google Scholar 

  124. Smolka, M. et al. Comprehensive structural variant detection: from mosaic to population-level. Preprint at bioRxiv https://doi.org/10.1101/2022.04.04.487055 (2022).

  125. Sedlazeck, F. J. et al. Accurate detection of complex structural variations using single-molecule sequencing. Nat. Methods 15, 461–468 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Ebler, J. et al. Pangenome-based genome inference allows efficient and accurate genotyping across a wide spectrum of variant classes. Nat. Genet. 54, 518–525 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Shen, W., Le, S., Li, Y. & Hu, F. SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS ONE 11, e0163962 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  129. Dale, R. K., Pedersen, B. S. & Quinlan, A. R. Pybedtools: a flexible Python library for manipulating genomic datasets and annotations. Bioinformatics 27, 3423–3424 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Virtanen, P. et al. SciPy 1.0: fundamental algorithms for scientific computing in Python. Nat. Methods 17, 261–272 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Cock, P. J. A. et al. Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25, 1422–1423 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the High-Performance Research Computing Center at Texas A&M University for support. DNA library preparation and long-read sequencing were performed at the University of Maryland Institute for Genome Sciences (L. Tallon and L. Sadzewicz). Illumina sequencing was performed through the Texas A&M Institute for Genome Sciences & Society research core (A. Hillhouse). We thank R. Stanyon for the flow-sorted domestic cat chromosomes for FISH experiments. This research was supported by grants from the Morris Animal Foundation (grant D19FE-04 to W.J.M. and W.C.W.), the National Science Foundation (grants DEB-1753760 and DEB-2150664 to W.J.M.) and the National Institutes of Health (NIH; grant R01 GM59290 to M.A.B.). A.J.H. was funded, in part, by a training grant from the National Institute of General Medical Sciences, NIH (T32 GM135115). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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Author notes

  1. These authors contributed equally: Kevin R. Bredemeyer, LaDeana Hillier, Andrew J. Harris.

Authors and Affiliations

  1. Veterinary Integrative Biosciences, Texas A&M University, College Station, TX, USA

    Kevin R. Bredemeyer, Andrew J. Harris, Nicole M. Foley, Brian W. Davis, Terje Raudsepp & William J. Murphy

  2. Interdisciplinary Program in Genetics & Genomics, Texas A&M University, College Station, TX, USA

    Kevin R. Bredemeyer, Andrew J. Harris, Brian W. Davis, Terje Raudsepp & William J. Murphy

  3. Department of Genome Sciences, University of Washington, Seattle, WA, USA

    LaDeana Hillier

  4. School of Biology & Environmental Sciences, University College Dublin, Dublin, Ireland

    Graham M. Hughes & Colleen Lawless

  5. Department of Animal Sciences, University of Missouri, Columbia, MO, USA

    Rachel A. Carroll, Edward S. Rice & Wesley C. Warren

  6. Institute for Systems Biology, Seattle, WA, USA

    Jessica M. Storer

  7. Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, USA

    Mark A. Batzer

  8. Guy Harvey Oceanographic Center, Nova Southeastern University, Fort Lauderdale, FL, USA

    Stephen J. O’Brien

  9. Department of Veterinary Medicine & Surgery, University of Missouri, Columbia, MO, USA

    Leslie A. Lyons

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Contributions

W.J.M. and W.C.W. were responsible for conceptualizing the project. K.R.B., L.H., A.J.H., G.H., N.M.F., C.L., R.C., J.M.S., E.R., B.W.D., T.R., L.A.L. and S.J.O. developed the methodology. K.R.B., L.H., A.J.H., N.M.F., G.H. and T.R. were involved in data visualization. Funding for the project was acquired by W.J.M. and W.C.W. W.J.M. and W.C.W. were responsible for project administration. Supervision of the project was provided by W.J.M., W.C.W. and M.A.B. The original draft of the manuscript was prepared by W.J.M., K.R.B., L.H., A.J.H., G.H., N.M.F. and W.C.W. All authors contributed to the investigation phase of the study and participated in the review and editing of the manuscript.

Corresponding authors

Correspondence to Wesley C. Warren or William J. Murphy.

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Bredemeyer, K.R., Hillier, L., Harris, A.J. et al. Single-haplotype comparative genomics provides insights into lineage-specific structural variation during cat evolution. Nat Genet 55, 1953–1963 (2023). https://doi.org/10.1038/s41588-023-01548-y

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