CoChat
Sign Up
Cited by 13Genetic and Clinical Aspects of Sex Determination and Chromosomal AbnormalitiesChromosomal and Genetic VariationsSperm and Testicular Function

Rapid Macrosatellite Evolution Promotes X-Linked Hybrid Male Sterility in a Feline Interspecies Cross

Open access
Bredemeyer, Kevin R, Seabury, Christopher M, Stickney, Mark J, McCarrey, John R, vonHoldt, Bridgett M, Murphy, William J·2021·Molecular Biology and Evolution
DOI 10.1093/molbev/msab274PMC PMC8662614
Open this paper in CoChat — free account

Abstract

The sterility or inviability of hybrid offspring produced from an interspecific mating result from incompatibilities between parental genotypes that are thought to result from divergence of loci involved in epistatic interactions. However, attributes contributing to the rapid evolution of these regions also complicates their assembly, thus discovery of candidate hybrid sterility loci is difficult and has been restricted to a small number of model systems. Here we reported rapid interspecific divergence at the DXZ4 macrosatellite locus in an interspecific cross between two closely related mammalian species: the domestic cat (Felis silvestris catus) and the Jungle cat (Felis chaus). DXZ4 is an interesting candidate due to its structural complexity, copy number variability, and described role in the critical yet complex biological process of X-chromosome inactivation. However, the full structure of DXZ4 was absent or incomplete in nearly every available mammalian genome assembly given its repetitive complexity. We compared highly continuous genomes for three cat species, each containing a complete DXZ4 locus, and discovered that the felid DXZ4 locus differs substantially from the human ortholog, and that it varies in copy number between cat species. Additionally, we reported expression, methylation, and structural conformation profiles of DXZ4 and the X chromosome during stages of spermatogenesis that have been previously associated with hybrid male sterility. Collectively, these findings suggest a new role for DXZ4 in male meiosis and a mechanism for feline interspecific incompatibility through rapid satellite divergence.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1093/molbev/msab274

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Comparative genomic evidence in cats and house mice suggests that some regions on the X chromosome are 'protected' from recombination, causing hybrid male offspring to be sterile if altered, thereby reinforcing the distinction among lineages.

    “For example, comparative genomic evidence in cats (Bredemeyer et al. 2021) and house mice (Forejt et al. 2021) suggests that some regions on the X chromosome are “protected” from recombination, causing hybrid male offspring to be sterile if altered, thereby reinforcing the distinction among lineages.”

    From How many mammal species are there now? Updates and trends in taxonomic, nomenclatural, and geographic knowledge (2025) · cites this paper as Bredemeyer et al. 2021

    Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 154

  1. Akalin A, Kormaksson M, Li S, Garrett-Bakelman FE, Figueroa ME, Melnick A, Mason CE. 2012. MethylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biol. 13:R87. PMC3491415 23034086
  2. Alavattam KG, Maezawa S, Sakashita A, Khoury H, Barski A, Kaplan N, Namekawa SH. 2019. Attenuated chromatin compartmentalization in meiosis and its maturation in sperm development. Nat Struct Mol Biol. 26(3): 175– 184. 30778237 PMC6402993
  3. Allen R, Ryan H, Davis BW, King C, Frantz L, Irving-Pease E, Barnett R, Linderholm A, Loog L, Haile J, et al 2020. A mitochondrial genetic divergence proxy predicts the reproductive compatibility of mammalian hybrids: a mitochondrial proxy of hybridibility. Proc R Soc B Biol Sci. 287: 20200690. PMC7341909 32486979
  4. Alonge M, Soyk S, Ramakrishnan S, Wang X, Goodwin S, Sedlazeck FJ, Lippman ZB, Schatz MC. 2019. RaGOO: fast and accurate reference-guided scaffolding of draft genomes. Genome Biol. 20(1): 224. 31661016 PMC6816165
  5. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215(3): 403– 410. 2231712
  6. Anders S, McCarthy DJ, Chen Y, Okoniewski M, Smyth GK, Huber W, Robinson MD. 2013. Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nat Protoc. 8(9): 1765– 1786. 23975260
  7. Antunes A, Pontius J, Ramos MJ, O'Brien SJ, Johnson WE. 2007. Mitochondrial introgressions into the nuclear genome of the domestic cat. J Hered. 98(5): 414– 420. 17660503
  8. Armstrong SJ, Hultén MA, Keohane AM, Turner BM. 1997. Different strategies of X-inactivation in germinal and somatic cells: histone H4 underacetylation does not mark the inactive X chromosome in the mouse male germline. Exp Cell Res. 230(2): 399– 402. [Internet] 9024800
  9. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al 2000. Gene ontology: tool for the unification of biology. Nat Genet. 25(1): 25– 29. 10802651 PMC3037419
  10. Assaad FF, Tucker KL, Signer ER. 1993. Epigenetic repeat-induced gene silencing (RIGS) in Arabidopsis. Plant Mol Biol. 22(6): 1067– 1085. 8400126
  11. Axtell MJ. 2013. ShortStack: comprehensive annotation and quantification of small RNA genes. RNA 19(6): 740– 751. 23610128 PMC3683909
  12. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME Suite: tools for motif discovery and searching. Nucleic Acids Res. 37(Web Server issue): W202– W208. 19458158 PMC2703892
  13. Bansal P, Kondaveeti Y, Pinter SF. 2019. Forged by DXZ4, FIRRE, and ICCE: how tandem repeats shape the active and inactive X chromosome. Front Cell Dev Biol. 7: 328– 310. 32076600 PMC6985041
  14. Barr ML, Bertram EG. 1949. A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature 163(4148): 676– 677. 18120749
  15. Bayes JJ, Malik HS. 2009. Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 326(5959): 1538– 1541. 19933102 PMC2987944
  16. Beissinger TM, Rosa GJ, Kaeppler SM, Gianola D, De Leon N. 2015. Defining window-boundaries for genomic analyses using smoothing spline techniques. Genet Sel Evol. 47: 30. 25928167 PMC4404117
  17. Bhattacharyya T, Gregorova S, Mihola O, Anger M, Sebestova J, Denny P, Simecek P, Forejt J. 2013. Mechanistic basis of infertility of mouse intersubspecific hybrids. Proc Natl Acad Sci U S A. 110(6): E468– 477. 23329330 PMC3568299
  18. Bhattacharyya T, Reifova R, Gregorova S, Simecek P, Gergelits V, Mistrik M, Martincova I, Pialek J, Forejt J. 2014. X chromosome control of meiotic chromosome synapsis in mouse inter-subspecific hybrids. PLoS Genet. 10(2): e1004088. 24516397 PMC3916230
  19. Bonora G, Deng X, Fang H, Ramani V, Qiu R, Berletch JB, Filippova GN, Duan Z, Shendure J, Noble WS, et al 2018. Orientation-dependent Dxz4 contacts shape the 3D structure of the inactive X chromosome. Nat Commun. 9(1): 1445. [Internet] 29654302 PMC5899087
  20. Bourgeois CA, Laquerriere F, Hemon D, Hubert J, Bouteille M. 1985. New data on the in situ position of the inactive X chromosome in the interphase nucleus of human fibroblasts. Hum Genet. 69(2): 122– 129. 3972413
  21. Boyle P, Clement K, Gu H, Smith ZD, Ziller M, Fostel JL, Holmes L, Meldrim J, Kelley F, Gnirke A, et al 2012. Gel-free multiplexed reduced representation bisulfite sequencing for large-scale DNA methylation profiling. Genome Biol. 13(10): R92. 23034176 PMC3491420
  22. Brashear WA, Bredemeyer KR, Murphy WJ. 2021. Structural and functional constraints dominated placental mammal X chromosome evolution. Genome Res. 31(8): 1353– 1365. 34301625 PMC8327908
  23. Brashear WA, Raudsepp T, Murphy WJ. 2018. Evolutionary conservation of Y chromosome ampliconic gene families despite extensive structural variation. Genome Res. 28(12): 1841– 1840. 30381290 PMC6280758
  24. Bredemeyer KR, Harris AJ, Li G, Zhao L, Foley NM, Roelke-Parker M, O'Brien SJ, Lyons LA, Warren WC, Murphy WJ. 2021. Ultracontinuous single haplotype genome assemblies for the domestic cat (Felis catus) and Asian Leopard Cat (Prionailurus bengalensis). J Hered. 112(2): 165– 173. 33305796 PMC8006817
  25. Brockdorff N, Turner BM. 2015. Dosage compensation in mammals. Cold Spring Harb Perspect Biol. 7(3): a019406. 25731764 PMC4355265
  26. Buckley RM, Davis BW, Brashear WA, Farias FHG, Kuroki K, Graves T, Hillier LDW, Kremitzki M, Li G, Middleton RP. 2020. 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. 33090996 PMC7581003
  27. Burgoyne PS, Mahadevaiah SK, Turner JMA. 2009. The consequences of asynapsis for mammalian meiosis. Nat Rev Genet. 10(3): 207– 216. 19188923
  28. Campbell P, Good JM, Nachman MW. 2013. Meiotic sex chromosome inactivation is disrupted in sterile hybrid male house mice. Genetics 193(3): 819– 828. 23307891 PMC3584000
  29. Chadwick BP. 2008. 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(8): 1259– 1269. 18456864 PMC2493436
  30. Chadwick BP. 2009. Macrosatellite epigenetics: the two faces of DXZ4 and D4Z4. Chromosoma 118(6): 675– 681. 19690880
  31. Chadwick BP, Willard HF. 2003. Chromatin of the Barr body: histone and non-histone proteins associated with or excluded from the inactive X chromosome. Hum Mol Genet. 12(17): 2167– 2178. 12915472
  32. Chen PY, Cokus SJ, Pellegrini M. 2010. BS Seeker: precise mapping for bisulfite sequencing. BMC Bioinformatics 11: 203– 206. 20416082 PMC2871274
  33. Coyne JA, Orr HA. 1997. Patterns of speciation in Drosophila. Evolution (NY). 51(1): 295. 28568795
  34. Coyne JA. 1992. Genetics and speciation. Nature 355(6360): 511– 515. 1741030
  35. Coyne JA. 2018. “Two rules of speciation” revisited. Mol Ecol. 27(19): 3749– 3752. 29972891
  36. Craven P, Wahba G. 1978. Smoothing noisy data with spline functions. Numer Math. 31(4): 377– 403.
  37. Darrow EM, Huntley MH, Dudchenko O, Stamenova EK, Durand NC, Sun Z, Huang SC, Sanborn AL, Machol I, Shamim M, et al 2016. Deletion of DXZ4 on the human inactive X chromosome alters higher-order genome architecture. Proc Natl Acad Sci U S A. 113(31): E4504– E4512. 27432957 PMC4978254
  38. Davis BW, Seabury CM, Brashear WA, Li G, Roelke-Parker M, Murphy WJ. 2015. Mechanisms underlying mammalian hybrid sterility in two feline interspecies models. Mol Biol Evol. 32(10): 2534– 2546. 26006188 PMC4592343
  39. Deng X, Ma W, Ramani V, Hill A, Yang F, Ay F, Berletch JB, Blau CA, Shendure J, Duan Z, et al 2015. Bipartite structure of the inactive mouse X chromosome. Genome Biol. 16: 152– 121. 26248554 PMC4539712
  40. Dhanoa JK, Sethi RS, Verma R, Arora JS, Mukhopadhyay CS. 2018. Long non-coding RNA: its evolutionary relics and biological implications in mammals: a review. J Anim Sci Technol. 60: 25.[Internet] 30386629 PMC6201556
  41. Dobin A, Gingeras TR, Spring C, Flores R, Sampson J, Knight R, Chia N, Technologies HS. 2016. Mapping RNA-seq with STAR. Curr Protoc Bioinformatics 51: 586– 597. PMC4631051 26334920
  42. Dudchenko O, Batra SS, Omer AD, Nyquist SK, Hoeger M, Durand NC, Shamim MS, Machol I, Lander ES, Aiden AP, et al 2017. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science 356(6333): 92– 95. 28336562 PMC5635820
  43. Dumbovic G, Forcales SV, Perucho M. 2017. Emerging roles of macrosatellite repeats in genome organization and disease development. Epigenetics 12(7): 515– 526. 28426282 PMC5687341
  44. Durand NC, Robinson JT, Shamim MS, Machol I, Mesirov JP, Lander ES, Aiden EL. 2016. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst. 3(1): 99– 101. 27467250 PMC5596920
  45. Durand NC, Shamim MS, Machol I, Rao SSP, Huntley MH, Lander ES, Aiden EL. 2016. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 3(1): 95– 98. 27467249 PMC5846465
  46. Durbin R, Eddy S, Krogh A, Mitchison G. 1998. Biological sequence analysis: probabilistic models of proteins and nucleic acids. Cambridge: Cambridge University Press.
  47. Dyer KA, Canfield TK, Gartler SM. 1989. Molecular cytological differentiation of active from inactive X domains in interphase: implications for X chromosome inactivation. Cytogenet Cell Genet. 50(2 − 3): 116– 120. 2776476
  48. Fang H, Bonora G, Lewandowski JP, Thakur J, Filippova GN, Henikoff S, Shendure J, Duan Z, Rinn JL, Deng X, et al 2020. Trans- and cis-acting effects of Firre on epigenetic features of the inactive X chromosome. Nat Commun. 11(1): 6053. 33247132 PMC7695720
  49. Ferree PM, Barbash DA. 2009. Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol. 7(10): e1000234. 19859525 PMC2760206
  50. Ferree PM, Prasad S. 2012. How can satellite DNA divergence cause reproductive isolation? Let US COUNT THE CHROMOSOMAL Ways. Genet Res Int. 2012: 430136– 430111. 22567387 PMC3335601
  51. Figueroa DM, Darrow EM, Chadwick BP. 2015. 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(4): 733– 752. 26188586 PMC4668219
  52. Filippova GN. 2007. Genetics and epigenetics of the multifunctional protein CTCF. Curr Top Dev Biol. 80: 337– 360. 17950379
  53. Galupa R, Heard E. 2018. X-chromosome inactivation: a crossroads between chromosome architecture and gene regulation. Annu Rev Genet. 52: 535– 566. 30256677
  54. Ghurye J, Pop M, Koren S, Bickhart D, Chin CS. 2017. Scaffolding of long read assemblies using long range contact information. BMC Genomics 18(1): 527– 511. 28701198 PMC5508778
  55. Ghurye J, Rhie A, Walenz BP, Schmitt A, Selvaraj S, Pop M, Phillippy AM, Koren S. 2019. Integrating Hi-C links with assembly graphs for chromosome-scale assembly. PLoS Comput Biol. 15(8): e1007273.[Internet] 31433799 PMC6719893
  56. Giacalone J, Friedes J, Francke U. 1992. A novel GC–rich human macrosatellite VNTR in Xq24 is differentially methylated on active and inactive X chromosomes. Nat Genet. 1(2): 137– 143. 1302007
  57. Giorgetti L, Lajoie BR, Carter AC, Attia M, Zhan Y, Xu J, Chen CJ, Kaplan N, Chang HY, Heard E, et al 2016. Structural organization of the inactive X chromosome in the mouse. Nature 535(7613): 575– 579. 27437574 PMC5443622
  58. Go VL, Vernon RG, Fritz IB. 1971. Studies on spermatogenesis in rats. I. Application of the sedimentation velocity technique to an investigation of spermatogenesis. Can J Biochem. 49(7): 753– 760. 5557889
  59. Good JM, Dean MD, Nachman MW. 2008. A complex genetic basis to X-linked hybrid male sterility between two species of house mice. Genetics 179(4): 2213– 2228. 18689897 PMC2516092
  60. Good JM, Giger T, Dean MD, Nachman MW. 2010. Widespread over-expression of the X chromosome in sterile F1 hybrid mice. PLoS Genet. 6(9): e1001148. 20941395 PMC2947990
  61. Grant CE, Bailey TL, Noble WS. 2011. FIMO: scanning for occurrences of a given motif. Bioinformatics 27(7): 1017– 1018. 21330290 PMC3065696
  62. Graves JAM. 2006. Sex chromosome specialization and degeneration in mammals. Cell 124(5): 901– 914. 16530039
  63. Guan D, Guan D, McCarthy SA, Wood J, Howe K, Wang Y, Durbin R, Durbin R. 2020. Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics 36(9): 2896– 2898. 31971576 PMC7203741
  64. Handel MA. 2004. The XY body: a specialized meiotic chromatin domain. Exp Cell Res. 296(1): 57– 63. 15120994
  65. Harris RS. 2007. Improved pairwise alignment of genomic DNA [PhD thesis]. State College (PA): The Pennsylvania State University.
  66. Henikoff S. 1998. Conspiracy of silence among repeated transgenes. Bioessays 20(7): 532– 535. 9723001
  67. Hewitt JE, Lyle R, Clark LN, Valleley EM, Wright TJ, Wijmenga C, Van Deutekom J. T, Francis F, Sharpe PT, Hofker M. 1994. Analysis of the tandem repeat locus D4Z4 associated with facioscapulohumeral muscular dystrophy. Hum Mol Genet. 3(8): 1287– 1295. 7987304
  68. Horakova AH, Calabrese JM, McLaughlin CR, Tremblay DC, Magnuson T, Chadwick BP. 2012. The mouse DXZ4 homolog retains CTCF binding and proximity to Pls3 despite substantial organizational differences compared to the primate macrosatellite. Genome Biol. 13(8): R70. 22906166 PMC3491370
  69. Horakova AH, Moseley SC, Mclaughlin CR, Tremblay DC, Chadwick BP. 2012. The macrosatellite DXZ4 mediates CTCF-dependent long-range intrachromosomal interactions on the human inactive X chromosome. Hum Mol Genet. 21(20): 4367– 4377. 22791747 PMC3459461
  70. Hoyer-Fender S. 2003. Molecular aspects of XY body formation. Cytogenet Genome Res. 103(3-4): 245– 255. 15051945
  71. Hu J, Fan J, Sun Z, Liu S. 2020. NextPolish: a fast and efficient genome polishing tool for long-read assembly. Bioinformatics 36(7): 2253– 2255. 31778144
  72. Ishishita S, Tsuboi K, Ohishi N, Tsuchiya K, Matsuda Y. 2015. Abnormal pairing of X and y sex chromosomes during meiosis I in interspecific hybrids of Phodopus campbelli and P. sungorus. Sci Rep. 5: 1– 9. PMC4371188 25801302
  73. Jablonka E, Lamb MJ. 1991. Sex chromosomes and speciation. Proc R Soc B Biol Sci. 243: 203– 208. 1675798
  74. Jégu T, Aeby E, Lee JT. 2017. The X chromosome in space. Nat Rev Genet. 18(6): 377– 389. 28479596
  75. Johnson WE, Eizirik E, Pecon-Slattery J, Murphy WJ, Antunes A, Teeling E, O’Brien SJ. 2006. The late Miocene radiation of modern felidae: a genetic assessment. Science 311(5757): 73– 77. 16400146
  76. Kang HM, Sul JH, Service SK, Zaitlen NA, Kong SY, Freimer NB, Sabatti C, Eskin E. 2010. Variance component model to account for sample structure in genome-wide association studies. Nat Genet. 42(4): 348– 354. 20208533 PMC3092069
  77. Kierszenbaum AL, Tres LL. 1974. Nucleolar and perichromosomal RNA synthesis during meiotic prophase in the mouse testis. J Cell Biol. 60(1): 39– 53. 4203361 PMC2109138
  78. Kim J-H, Antunes A, Luo S-J, Menninger J, Nash WG, O'Brien SJ, Johnson WE. 2006. Evolutionary analysis of a large mtDNA translocation (numt) into the nuclear genome of the Panthera genus species. Gene 366(2): 292– 302. 16380222 PMC1592465
  79. Knibiehler B, Mirre C, Hartung M, Jean P, Stahl A, Delanversin A, Soler M. 1981. Sex vesicle-associated nucleolar organizers in mouse spermatocytes: localization, structure, and function. Cytogenet Cell Genet. 31(2): 47– 57. 7307582
  80. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 35(6): 1547– 1549. 29722887 PMC5967553
  81. Kutter C, Watt S, Stefflova K, Wilson MD, Goncalves A, Ponting CP, Odom DT, Marques AC. 2012. Rapid turnover of long noncoding RNAs and the evolution of gene expression. PLoS Genet. 8(7): e1002841. 22844254 PMC3406015
  82. Lahn BT, Page DC. 1999. Four evolutionary strata on the human X chromosome. Science 286(5441): 964– 967. 10542153
  83. Langmead B. 2010. Aligning short sequencing reads with Bowtie. Curr Protoc Bioinformatics. 32: 11.7.1–11.7.4. PMC3010897 21154709
  84. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods. 9(4): 357– 359. 22388286 PMC3322381
  85. Larson EL, Keeble S, Vanderpool D, Dean MD, Good JM. 2016. The composite regulatory basis of the large X-effect in mouse speciation. Mol Biol Evol. 34: 282– 295. PMC6200130 27999113
  86. Lea AJ, Tung J, Zhou X. 2015. A flexible, efficient binomial mixed model for identifying differential DNA methylation in bisulfite sequencing data. PLoS Genet. 11(11): e1005650. 26599596 PMC4657956
  87. Lifschytz E, Lindsley DL. 1972. The role of X-chromosome inactivation during spermatogenesis (Drosophila-allocycly-chromosome evolution-male sterility-dosage compensation). Proc Natl Acad Sci U S A. 69(1): 182– 186. 4621547 PMC427571
  88. Li G, Davis BW, Eizirik E, Murphy WJ. 2016. Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae). Genome Res. 26(1): 1– 11. PMC4691742 26518481
  89. Li G, Davis BW, Raudsepp T, Pearks Wilkerson AJ, Mason VC, Ferguson-Smith M, O’Brien PC, Waters PD, Murphy WJ. 2013. Comparative analysis of mammalian y chromosomes illuminates ancestral structure and lineage-specific evolution. Genome Res. 23(9): 1486– 1495. 23788650 PMC3759724
  90. Li G, Hillier LW, Grahn RA, Zimin AV, David VA, Menotti-Raymond M, Middleton R, Hannah S, Hendrickson S, Makunin A, et al 2016. A high-resolution SNP array-based linkage map anchors a new domestic cat draft genome assembly and provides detailed patterns of recombination. G3 (Bethesda) 6(6): 1607– 1616. 27172201 PMC4889657
  91. Li G, Figueiró HV, Eizirik E, Murphy WJ, Yoder A. 2019. Recombination-aware phylogenomics reveals the structured genomic landscape of hybridizing cat species. Mol Biol Evol. 36(10): 2111– 2126. 31198971 PMC6759079
  92. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25(14): 1754– 1760. 19451168 PMC2705234
  93. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25(16): 2078– 2079. 19505943 PMC2723002
  94. Liu WS. 2019. Mammalian sex chromosome structure, gene content, and function in male fertility. Annu Rev Anim Biosci. 7: 103– 124. 30412673
  95. Lopez JV, Cevario S, O'Brien SJ. 1996. Complete nucleotide sequences of the domestic cat (Felis catus) mitochondrial genome and a transposed mtDNA tandem repeat (Numt) in the nuclear genome. Genomics 33(2): 229– 246. 8660972
  96. Lucotte EA, Skov L, Jensen JM, Macià MC, Munch K, Schierup MH. 2018. Dynamic copy number evolution of X-and Y-linked ampliconic genes in human populations. Genetics 209(3): 907– 920. [Internet] 29769284 PMC6028258
  97. Lustyk D, Kinský S, Ullrich KK, Yancoskie M, Kašíková L, Gergelits V, Sedlacek R, Chan YF, Odenthal-Hesse L, Forejt J, et al 2019. Genomic structure of Hstx2 modifier of Prdm9-dependent hybrid male sterility in mice. Genetics 213(3): 1047– 1063. 31562180 PMC6827376
  98. Lyon MF. 1961. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190: 372– 373. 13764598
  99. Marçais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, Zimin A. 2018. MUMmer4: a fast and versatile genome alignment system. PLoS Comput Biol. 14(1): e1005944. 29373581 PMC5802927
  100. Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17(1): 10– 12.
  101. Masly JP, Presgraves DC. 2007. High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biol. 5(9): e243. 17850182 PMC1971125
  102. McCarrey JR, Berg WM, Paragioudakis SJ, Zhang PL, Dilworth DD, Arnold BL, Rossi JJ. 1992. Differential transcription of Pgk genes during spermatogenesis in the mouse. Dev Biol. 154(1): 160– 168. 1426623
  103. McCarthy DJ, Chen Y, Smyth GK. 2012. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 40(10): 4288– 4297. 22287627 PMC3378882
  104. McKee BD, Handel MA. 1993. Sex chromosomes, recombination, and chromatin conformation. Chromosoma 102(2): 71– 80. 8432196
  105. McLaughlin CR, Chadwick BP. 2011. Characterization of DXZ4 conservation in primates implies important functional roles for CTCF binding, array expression and tandem repeat organization on the X chromosome. Genome Biol. 12(4): R37. 21489251 PMC3218863
  106. Mi H, Muruganujan A, Ebert D, Huang X, Thomas PD. 2019. PANTHER version 14: more genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools. Nucleic Acids Res. 47(D1): D419– D426. 30407594 PMC6323939
  107. Miga KH, Koren S, Rhie A, Vollger MR, Gershman A, Bzikadze A, Brooks S, Howe E, Porubsky D, Logsdon GA, et al 2020. Telomere-to-telomere assembly of a complete human X chromosome. Nature 585(7823): 79– 84. 32663838 PMC7484160
  108. Mikheenko A, Prjibelski A, Saveliev V, Antipov D, Gurevich A. 2018. Bioinformatics Versatile genome assembly evaluation with QUAST-LG. Vol. 34. Oxford: Oxford University Press. p. i142– i150. 29949969 PMC6022658
  109. Moore CM, Janish C, Eddy CA, Hubbard GB, Leland MM, Rogers J. 1999. Cytogenetic and fertility studies of a Rheboon, rhesus macaque (Macaca mulatta) x baboon (Papio hamadryas) cross: further support for a single karyotype nomenclature. Am J Phys Anthropol. 110(2): 119– 127. 10502238
  110. Moretti C, Vaiman D, Tores F, Cocquet J. 2016. Expression and epigenomic landscape of the sex chromosomes in mouse post-meiotic male germ cells. Epigenetics Chromatin. 9: 47. 27795737 PMC5081929
  111. Murphy WJ, O'Brien SJ. 2007. Designing and optimizing comparative anchor primers for comparative gene mapping and phylogenetic inference. Nat Protoc. 2(11): 3022– 3030. 18007639
  112. Murphy WJ, Pearks Wilkerson AJ, Raudsepp T, Agarwala R, Schaffer AA, Stanyon R, Chowdhary BP. 2006. Novel gene acquisition on Carnivore Y chromosomes. PLoS Genet. 2(3): e43. 16596168 PMC1420679
  113. Namekawa SH, Park PJ, Zhang LF, Shima JE, McCarrey JR, Griswold MD, Lee JT. 2006. Postmeiotic sex chromatin in the male germline of mice. Curr Biol. 16(7): 660– 667. 16581510
  114. Nattestad M, Schatz MC. 2016. Assemblytics: a web analytics tool for the detection of variants from an assembly. Bioinformatics 32(19): 3021– 3023. 27318204 PMC6191160
  115. Ogaki Y, Fukuma M, Shimizu N. 2020. Repeat induces not only gene silencing, but also gene activation in mammalian cells. PLoS One. 15(6): e0235127. 32579599 PMC7313748
  116. Patel L, Kang R, Rosenberg SC, Qiu Y, Raviram R, Chee S, Hu R, Ren B, Cole F, Corbett KD. 2019. Dynamic reorganization of the genome shapes the recombination landscape in meiotic prophase. Nat Struct Mol Biol. 26(3): 164– 174. 30778236 PMC6403010
  117. Pearks Wilkerson AJ, Raudsepp T, Graves T, Albracht D, Warren W, Chowdhary BP, Skow LC, Murphy WJ. 2008. Gene discovery and comparative analysis of X-degenerate genes from the domestic cat Y chromosome. Genomics 92(5): 329– 338. 18674610
  118. Pohlers M, Mauro Calabrese J, Magnuson T. 2014. Small RNA expression from the human macrosatellite DXZ4. G3 (Bethesda) 4(10): 1981– 1989. 25147189 PMC4199704
  119. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26(6): 841– 842. 20110278 PMC2832824
  120. Ramani V, Cusanovich DA, Hause RJ, Ma W, Qiu R, Deng X, Blau CA, Disteche CM, Noble WS, Shendure J, et al 2016. Mapping 3D genome architecture through in situ DNase Hi-C. Nat Protoc. 11(11): 2104– 2121. 27685100 PMC5547819
  121. Ramírez-Colmenero A, Oktaba K, Fernandez-Valverde SL. 2020. Evolution of genome-organizing long non-coding RNAs in metazoans. Front Genet. 11: 589697. 33329735 PMC7734150
  122. Rao SSP, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, Robinson JT, Sanborn AL, Machol I, Omer AD, Lander ES, et al 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159(7): 1665– 1680. 25497547 PMC5635824
  123. Rhie A, McCarthy SA, Fedrigo O, Damas J, Formenti G, Koren S, Uliano-Silva M, Chow W, Fungtammasan A, Gedman GL, et al 2020. Towards complete and error-free genome assemblies of all vertebrate species. bioRxiv [Internet] 52:2020.05.22.110833. PMC8081667 33911273
  124. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1): 139– 140. 19910308 PMC2796818
  125. Royo H, Polikiewicz G, Mahadevaiah SK, Prosser H, Mitchell M, Bradley A, De Rooij DG, Burgoyne PS, Turner JMA. 2010. Evidence that meiotic sex chromosome inactivation is essential for male fertility. Curr Biol. 20(23): 2117– 2123. 21093264
  126. Schaap M, Lemmers RJLF, Maassen R, van der Vliet PJ, Hoogerheide LF, van Dijk HK, Baştürk N, de Knijff P, van der Maarel SM. 2013. Genome-wide analysis of macrosatellite repeat copy number variation in worldwide populations: evidence for differences and commonalities in size distributions and size restrictions. BMC Genomics 14: 143. 23496858 PMC3599962
  127. Schimenti J. 2005. Synapsis or silence. Nat Genet. 37(1): 11– 13. 15624015
  128. Schwahn DJ, Wang RJ, White MA, Payseur BA. 2018. Genetic dissection of hybrid male sterility across stages of spermatogenesis. Genetics 210(4): 1453– 1465. 30333190 PMC6283182
  129. Seabury CM, Oldeschulte DL, Saatchi M, Beever JE, Decker JE, Halley YA, Bhattarai EK, Molaei M, Freetly HC, Hansen SL, et al 2017. Genome-wide association study for feed efficiency and growth traits in U.S. beef cattle. BMC Genomics 18(1): 386. 28521758 PMC5437562
  130. Segura V, Vilhjálmsson BJ, Platt A, Korte A, Seren Ü, Long Q, Nordborg M. 2012. An efficient multi-locus mixed-model approach for genome-wide association studies in structured populations. Nat Genet. 44(7): 825– 830. 22706313 PMC3386481
  131. Shumate A, Salzberg SL. 2020. Liftoff: an accurate gene annotation mapping tool. bioRxiv [Internet]:2020.06.24.169680.
  132. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. 2015. BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31(19): 3210– 3212. 26059717
  133. Solari AJ. 1974. The behavior of the XY pair in mammals. Int Rev Cytol. 38(0): 273– 317. 4854664
  134. Sosa E, Flores L, Yan W, McCarrey JR. 2015. Escape of X-linked miRNA genes from meiotic sex chromosome inactivation. Development 142: 3791– 3800. 26395485 PMC4647214
  135. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9): 1312– 1313. 24451623 PMC3998144
  136. Tange O. 2011. GNU parallel: the command-line power tool. USENIX Mag. 42– 47.
  137. Thomsen PD, Schauser K, Bertelsen MF, Vejlsted M, Grøndahl C, Christensen K. 2011. Meiotic studies in infertile domestic pig-babirusa hybrids. Cytogenet Genome Res. 132(1 − 2): 124– 128. [Internet] 20924163
  138. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 7(3): 562– 578. 22383036 PMC3334321
  139. Tremblay DC, Moseley S, Chadwick BP. 2011. Variation in array size, monomer composition and expression of the macrosatellite DXZ4. PLoS One 6(4): e18969. 21544201 PMC3081327
  140. Turner JMA, Burgoyne PS, Singh PB. 2001. M31 and macroH2A1.2 colocalise at the pseudoautosomal region during mouse meiosis. J Cell Sci. 114(18): 3367– 3375. 11591824
  141. Turner JMA, Mahadevaiah SK, Fernandez-Capetillo O, Nussenzweig A, Xu X, Deng CX, Burgoyne PS. 2005. Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet. 37(1): 41– 47. 15580272
  142. Turner JMA. 2007. Meiotic sex chromosome inactivation. Development 134(10): 1823– 1831. 17329371
  143. Turner LM, White MA, Tautz D, Payseur BA. 2014. Genomic networks of hybrid sterility. PLoS Genet. 10(2): e1004162. 24586194 PMC3930512
  144. Turner LM, Harr B. 2014. Genome-wide mapping in a house mouse hybrid zone reveals hybrid sterility loci and Dobzhansky-Muller interactions. Elife 3: 2504. PMC4359376 25487987
  145. Van Overveld PGM, Lemmers RJFL, Sandkuijl LA, Enthoven L, Winokur ST, Bakels F, Padberg GW, Van Ommen GJB, Frants RR, Van Der Maarel SM. 2003. Hypomethylation of D4Z4 in 4q-linked and non-4q-linked facioscapulohumeral muscular dystrophy. Nat Genet. 35(4): 315– 317. 14634647
  146. Vernet N, Mahadevaiah SK, de Rooij DG, Burgoyne PS, Ellis PJI. 2016. Zfy genes are required for efficient meiotic sex chromosome inactivation (MSCI) in spermatocytes. Hum Mol Genet. 25(24): 5300– 5310. 27742779 PMC5418838
  147. de Vries M, Vosters S, Merkx G, D'Hauwers K, Wansink DG, Ramos L, de Boer P. 2012. Human male meiotic sex chromosome inactivation. PLoS One 7(2): e31485. 22355370 PMC3280304
  148. Wang H, Höög C. 2006. Structural damage to meiotic chromosomes impairs DNA recombination and checkpoint control in mammalian oocytes. J Cell Biol. 173(4): 485– 495. 16717125 PMC2063859
  149. Wang PJ, McCarrey JR, Yang F, Page DC. 2001. An abundance of X-linked genes expressed in spermatogonia. Nat Genet. 27(4): 422– 426. 11279525
  150. Wellcome Trust Case Control Consortium. 2007. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447:661–678. PMC2719288 17554300
  151. Yan W, McCarrey JR. 2009. Sex chromosome inactivation in the male. Epigenetics 4(7): 452– 456. 19838052 PMC3052906
  152. Yang F, Deng X, Ma W, Berletch JB, Rabaia N, Wei G, Moore JM, Filippova GN, Xu J, Liu Y, et al 2015. The lncRNA Firre anchors the inactive X chromosome to the nucleolus by binding CTCF and maintains H3K27me3 methylation. Genome Biol. 16: 52. 25887447 PMC4391730
  153. Yunis JJ, Yasmineh WG. 1971. Heterochromatin, satellite DNA, and cell function. Structural DNA of eukaryotes may support and protect genes and aid in speciation. Science 174(4015): 1200– 1209. 4943851
  154. Zhang LF, Huynh KD, Lee JT. 2007. Perinucleolar targeting of the inactive X during S phase: evidence for a role in the maintenance of silencing. Cell 129(4): 693– 706. 17512404

Cited by

Sorted by citations

Authors
Bredemeyer, K. R., Seabury, C. M., Stickney, M. J., McCarrey, J. R., vonHoldt, B. M., & Murphy, W. J.
Affiliations
  • Texas A&M University (US)
  • The University of Texas at San Antonio (US)
  • Princeton University (US)
Corresponding author
Murphy, William J
ORCID
Venue
Molecular Biology and Evolution
Publisher
Oxford University Press (OUP)
Published
2021-09-14
Volume
38
Issue
12
Pages
5588-5609
ISSN
  • 0737-4038 (ISSN-L)
  • 1537-1719
DOI
10.1093/molbev/msab274
PMC
PMC8662614
OpenAlex
W3199481410
Cited by
13
References
2
Citations by year
2026: 1 · 2025: 3 · 2024: 4 · 2023: 4 · 2021: 1
FWCI
1.27
Type
journal article
Language
en
Open access
Licence
Locations
  • Molecular Biology and Evolution (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • Morris Animal Foundation (D19FE-004)
  • National Science Foundation (DEB-1753760)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
Keywords
hybrid male sterility, interspecific hybridization, cats, jungle cat, Felis chaus, X chromosome inactivation, copy number variation, satellite DNA evolution, X chromosome methylation, spermatogenesis, male meiosis
MeSH terms
Animals, Cats, Infertility, Male, Male, X Chromosome, Genome, Felidae, X Chromosome Inactivation

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review