Human Genetics

, Volume 136, Issue 5, pp 511–528 | Cite as

The Y chromosomes of the great apes

Review
Part of the following topical collections:
  1. Y-Chromosome

Abstract

The great apes (orangutans, gorillas, chimpanzees, bonobos and humans) descended from a common ancestor around 13 million years ago, and since then their sex chromosomes have followed very different evolutionary paths. While great-ape X chromosomes are highly conserved, their Y chromosomes, reflecting the general lability and degeneration of this male-specific part of the genome since its early mammalian origin, have evolved rapidly both between and within species. Understanding great-ape Y chromosome structure, gene content and diversity would provide a valuable evolutionary context for the human Y, and would also illuminate sex-biased behaviours, and the effects of the evolutionary pressures exerted by different mating strategies on this male-specific part of the genome. High-quality Y-chromosome sequences are available for human and chimpanzee (and low-quality for gorilla). The chromosomes differ in size, sequence organisation and content, and while retaining a relatively stable set of ancestral single-copy genes, show considerable variation in content and copy number of ampliconic multi-copy genes. Studies of Y-chromosome diversity in other great apes are relatively undeveloped compared to those in humans, but have nevertheless provided insights into speciation, dispersal, and mating patterns. Future studies, including data from larger sample sizes of wild-born and geographically well-defined individuals, and full Y-chromosome sequences from bonobos, gorillas and orangutans, promise to further our understanding of population histories, male-biased behaviours, mutation processes, and the functions of Y-chromosomal genes.

References

  1. Agulnik AI, Zharkikh A, Boettger-Tong H, Bourgeron T, McElreavey K, Bishop CE (1998) Evolution of the DAZ gene family suggests that Y-linked DAZ plays little, or a limited, role in spermatogenesis but underlines a recent African origin for human populations. Hum Mol Genet 7:1371–1377. doi:10.1093/hmg/7.9.1371 PubMedCrossRefGoogle Scholar
  2. Arora N, Nater A, van Schaik CP, Willems EP, van Noordwijk MA, Goossens B, Morf N, Bastian M, Knott C, Morrogh-Bernard H, Kuze N, Kanamori T, Pamungkas J, Perwitasari-Farajallah D, Verschoor E, Warren K, Kruetzen M (2010) Effects of Pleistocene glaciations and rivers on the population structure of Bornean orangutans (Pongo pygmaeus) P Natl Acad Sci USA 107:21376-21381 doi:10.1073/pnas.1010169107
  3. Balaresque P, King TE, Parkin EJ, Heyer E, Carvalho-Silva D, Kraaijenbrink T, de Knijff P, Tyler-Smith C, Jobling MA (2014) Gene conversion violates the stepwise mutation model for microsatellites in y-chromosomal palindromic repeats. Hum Mutat 35:609–617. doi:10.1002/humu.22542 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Becquet C, Patterson N, Stone AC, Przeworski M, Reich D (2007) Genetic structure of chimpanzee populations. PLoS Genet. doi:10.1371/journal.pgen.0030066 PubMedPubMedCentralGoogle Scholar
  5. Bellott DW, Hughes JF, Skaletsky H, Brown LG, Pyntikova T, Cho TJ, Koutseva N, Zaghlul S, Graves T, Rock S, Kremitzki C, Fulton RS, Dugan S, Ding Y, Morton D, Khan Z, Lewis L, Buhay C, Wang Q, Watt J, Holder M, Lee S, Nazareth L, Alfoldi J, Rozen S, Muzny DM, Warren WC, Gibbs RA, Wilson RK, Page DC (2014) Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators. Nature 508:494–499. doi:10.1038/nature13206 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bernstein R, Wadee A, Rosendorff J, Wessels A, Jenkins T (1986) Inverted Y chromosome polymorphism in the Gujerati Muslim Indian population of South Africa. Hum Genet 74:223–229PubMedCrossRefGoogle Scholar
  7. Bhowmick BK, Satta Y, Takahata N (2007) The origin and evolution of human ampliconic gene families and ampliconic structure. Genome Res 17:441–450. doi:10.1101/gr.5734907 PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bosch E, Hurles ME, Navarro A, Jobling MA (2004) Dynamics of a human interparalog gene conversion hotspot. Genome Res 14:835–844. doi:10.1101/gr.2177404 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Brown GM, Furlong RA, Sargent CA, Erickson RP, Longepied G, Mitchell M, Jones MH, Hargreave TB, Cooke HJ, Affara NA (1998) Characterisation of the coding sequence and fine mapping of the human DFFRY gene and comparative expression analysis and manning to the Sxr(b) interval of the mouse Y chromosome of the Dffry gene. Hum Mol Genet 7:97–107PubMedCrossRefGoogle Scholar
  10. Burton ML, Moore CC, Whiting JWM, Romney AK (1996) Regions based on social structure Curr Anthropol 37:87–123. doi:10.1086/204474 CrossRefGoogle Scholar
  11. Carvalho CMB, Zhang F, Lupski JR (2011) Structural variation of the human genome: mechanisms, assays, and role in male infertility Syst Biol Reprod Mec 57:3–16 doi:10.3109/19396368.2010.527427
  12. Churchill JD, Schmedes SE, King JL, Budowle B (2016) Evaluation of the Illumina (R) Beta Version ForenSeq (TM) DNA Signature Prep Kit for use in genetic profiling Forensic Science International-Genetics 20:20–29 doi:10.1016/j.fsigen.2015.09.009
  13. Connallon T, Clark AG (2010) Gene duplication, gene conversion and the evolution of the Y chromosome Genetics 186:277-286 doi:10.1534/genetics.110.116756
  14. Cooke HJ, Brown WRA, Rappold GA (1985) Hypervariable telomeric sequences from the human sex-chromosomes are pseudoautosomal. Nature 317:687–692PubMedCrossRefGoogle Scholar
  15. Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A, Waters PD, Grutzner F, Kaessmann H (2014) Origins and functional evolution of Y chromosomes across mammals. Nature 508:488–493. doi:10.1038/nature13151 PubMedCrossRefGoogle Scholar
  16. Davis JK, Thomas PJ, Program NCS, Thomas JW (2010) A W-linked palindrome and gene conversion in New World sparrows and blackbirds Chromosome Res 18:543–553. doi:10.1007/s10577-010-9134-y PubMedGoogle Scholar
  17. de Manuel M, Kuhlwilm M, Frandsen P, Sousa VC, Desai T, Prado-Martinez J, Hernandez-Rodriguez J, Dupanloup I, Lao O, Hallast P, Schmidt JM, Heredia-Genestar JM, Benazzo A, Barbujani G, Peter BM, Kuderna LFK, Casals F, Angedakin S, Arandjelovic M, Boesch C, Kuhl H, Vigilant L, Langergraber K, Novembre J, Gut M, Gut I, Navarro A, Carlsen F, Andres AM, Siegismund HR, Scally A, Excoffier L, Tyler-Smith C, Castellano S, Xue YL, Hvilsom C, Marques-Bonet T (2016) Chimpanzee genomic diversity reveals ancient admixture with bonobos. Science 354:477–481. doi:10.1126/science.aag2602 PubMedCrossRefGoogle Scholar
  18. Delgado RA, Van Schaik CP (2000) The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): A tale of two islands. Evol Anthropol 9:201–218. doi:10.1002/1520-6505(2000)9:5<201:AID-EVAN2>3.0.CO;2-Y CrossRefGoogle Scholar
  19. Douadi MI, Gatti S, Levrero F, Duhamel G, Bermejo M, Vallet D, Menard N, Petit EJ (2007) Sex-biased dispersal in western lowland gorillas (Gorilla gorilla gorilla). Mol Ecol 16:2247–2259. doi:10.1111/j.1365-294X.2007.03286.x PubMedCrossRefGoogle Scholar
  20. Elsik CG, Tellam RL, Worley KC, Gibbs RA, Abatepaulo ARR, Abbey CA, Adelson DL, Aerts J, Ahola V, Alexander L, Alioto T, Almeida IG, Amadio AF, Anatriello E, Antonarakis SE, Anzola JM, Astashyn A, Bahadue SM, Baldwin CL, Barris W, Baxter R, Bell SN, Bennett AK, Bennett GL, Biase FH, Boldt CR, Bradley DG, Brinkman FSL, Brinkmeyer-Langford CL, Brown WC, Brownstein MJ, Buhay C, Caetano AR, Camara F, Carroll JA, Carvalho WA, Casey T, Cervelatti EP, Chack J, Chacko E, Chandrabose MM, Chapin JE, Chapple CE, Chen HC, Chen L, Cheng Y, Cheng Z, Childers CP, Chitko-McKown CG, Chiu R, Choi JW, Chrast J, Colley AJ, Connelley T, Cree A, Curry S, Dalrymple B, Diep Dao M, Davis C, de Oliveira CJF, de Miranda Santos IKF, de Campos TA, Deobald H, Devinoy E, Dickens CM, Ding Y, Dinh HH, De Donato M, Donohue KE, Donthu R, Dovc P, Dugan-Rocha S, Durbin KJ, Eberlein A, Edgar RC, Egan A, Eggen A, Eichler EE, Elhaik E, Ellis SA, Elnitski L, Ermolaeva O, Eyras E, Fitzsimmons CJ, Fowler GR, Franzin AM, Fritz K, Gabisi RA, Garcia GR, Garcia JF, Genini S, Gerlach D, German JB, Gilbert JGR, Gill CA, Gladney CJ, Glass EJ, Goodell J, Grant JR, Graur D, Greaser ML, Green JA, Green RD, Guan L, Guigo R, Hadsell DL, Hagen DE, Hakimov HA, Halgren R, Hamernik DL, Hamilton C, Harhay GP, Harrow JL, Hart EA, Hastings N, Havlak P, Henrichsen CN, Hernandez J, Hernandez M, Herzig CTA, Hiendleder SG, Hines S, Hitchens ME, Hlavina W, Hobbs M, Holder M, Holt RA, Hu ZL, Hume J, Iivanainen A, Ingham A, Iso-Touru T, Jamis C, Jann O, Jensen K, Jhangiani SN, Jiang HY, Johnson AJ, Jones SJM, Joshi V, Junier T, Kapetis D, Kappes SM, Kapustin Y, Keele JW, Kent MP, Kerr T, Khalil SS, Khatib H, Kiryutin B, Kitts P, Kokocinski F, Kolbehdari D, Kovar CL, Kriventseva EV, Kumar CG, Kumar D, Lahmers KK, Landrum M, Larkin DM, Lau LPL, Leach R, Lee JCM, Lee S, Lemay DG, Lewin HA, Lewis LR, Li CX, Lien S, Liu GE, Liu YS, Liu Y, Logan KM, Lopez J, Lozado RJ, Lutzow YS, Lynn DJ, MacNeil MD, Maglott D, Malinverni R, Maqbool NJ, Marques E, Marra MA, Martin WF, Martins NF, Maruyama SR, Matukumalli LK, Mazza R, McEwan JC, McKay SD, McLean KL, McWilliam S, Medrano JF, Memili E, Moen C, Molenaar AL, Moore SS, Moore R, More DD, Moreno BT, Morgan MB, Muntean CT, Muzny DM, Nandakumar HP, Nazareth LV, Nguyen NB, Nicholas FW, Nogueira MFG, Okwuonu GO, Olsaker I, Pant SD, Panzitta F, Pastor RCP, Patel BM, Payne GM, Plass M, Poli MA, Poslusny N, Pruitt K, Pu LL, Qin X, Rachagani S, Raison JM, Ranganathan S, Ratnakumar A, Razpet A, Reecy J, Reese JT, Ren Y, Reymond A, Riggs PK, Rijnkels M, Rincon G, Roberts A, Rodriguez-Osorio N, Rodriguez-Zas SL, Romero NE, Rosenwald A, Ruiz SJ, Sabo A, Salih H, Sando L, Santibanez J, Sapojnikov V, Schein JE, Schmutz SM, Schnabel RD, Schook L, Searle SM, Seo SW, Shen YF, Shen LB, Sherman L, Skow LC, Smith T, Snelling WM, Sodergren E, Solovyev V, Song H, Song JZ, Sonstegard TS, Southey BR, Souvorov A, Spurlock D, Steffen D, Stone RT, Stothard P, Sugimoto Y, Sweedler JV, Takasuga A, Tammen I, Taniguchi M, Taylor JF, Telugu BPVL, Ucla C, Urbanski JM, Utsunomiya YT, Van CP, Vattathil S, Verschoor CP, Waardenberg AJ, Walker A, Wang ZQ, Ward R, Warren JT, Waterman RC, Weikard R, Weinstock GM, Welsh TH, Wheeler DA, Wheeler TT, White SN, Whitside MD, Wilczek-Boney K, Williams JL, Williams RL, Wilming LG, Womack J, Wright RA, Wunderlich KR, Wyss C, Yang MQ, Yang JQ, Zdobnov EM, Zhang JK, Zhao FQ, Zhu B, Consortium BGSA (2009) The Genome Sequence of Taurine Cattle: A Window to Ruminant Biology and Evolution. Science 324:522–528. doi:10.1126/science.1169588 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Eriksson J, Hohmann G, Boesch C, Vigilant L (2004) Rivers influence the population genetic structure of bonobos (Pan paniscus). Mol Ecol 13:3425–3435. doi:10.1111/j.1365-294X.2004.02332.x PubMedCrossRefGoogle Scholar
  22. Eriksson J, Siedel H, Lukas D, Kayser M, Erler A, Hashimoto C, Hohmann G, Boesch C, Vigilant L (2006) Y-chromosome analysis confirms highly sex-biased dispersal and suggests a low male effective population size in bonobos (Pan paniscus). Mol Ecol 15:939–949. doi:10.1111/j.1365-294X.2006.02845.x PubMedCrossRefGoogle Scholar
  23. Ferlin A, Arredi B, Foresta C (2006) Genetic causes of male infertility. Reprod Toxicol 22:133–141. doi:10.1016/j.reprotox.2006.04.016 PubMedCrossRefGoogle Scholar
  24. Foresta C, Moro E, Rossi A, Rossato M, Garolla A, Ferlin A (2000) Role of the AZFa candidate genes in male infertility. J Endocrinol Invest 23:646–651. doi:10.1007/BF03343788 PubMedCrossRefGoogle Scholar
  25. Freije D, Helms C, Watson MS, Donis-Keller H (1992) Identification of a second pseudoautosomal region near the Xq and Yq telomeres. Science 258:1784–1787PubMedCrossRefGoogle Scholar
  26. Funfstuck T, Arandjelovic M, Morgan DB, Sanz C, Breuer T, Stokes EJ, Reed P, Olson SH, Cameron K, Ondzie A, Peeters M, Kuhl HS, Cipolletta C, Todd A, Masi S, Doran-Sheehy DM, Bradley BJ, Vigilant L (2014) The genetic population structure of wild Western Lowland Gorillas (Gorilla gorilla gorilla) living in continuous rain forest. Am J Primatol 76:868–878. doi:10.1002/ajp.22274 PubMedPubMedCentralCrossRefGoogle Scholar
  27. Genomes Project C, Auton A, Brooks LD, Durbin RM, Garrison EP, Kang HM, Korbel JO, Marchini JL, McCarthy S, McVean GA, Abecasis GR (2015) A global reference for human genetic variation. Nature 526:68–74. doi:10.1038/nature15393 CrossRefGoogle Scholar
  28. Glaser B, Grutzner F, Willmann U, Stanyon R, Arnold N, Taylor K, Rietschel W, Zeitler S, Toder R, Schempp W (1998) Simian Y Chromosomes: species-specific rearrangements of DAZ,RBM, and TSPY versus contiguity of PAR and SRY. Mamm Genome 9:226–231PubMedCrossRefGoogle Scholar
  29. Glazko GV, Nei M (2003) Estimation of divergence times for major lineages of primate species. Mol Biol Evol 20:424–434PubMedCrossRefGoogle Scholar
  30. Goto H, Peng L, Makova KD (2009) Evolution of X-degenerate Y chromosome genes in greater apes: conservation of gene content in human and Gorilla. But Not Chimpanzee J Mol Evol 68:134–144. doi:10.1007/s00239-008-9189-y PubMedCrossRefGoogle Scholar
  31. Graves JA (2006) Sex chromosome specialization and degeneration in mammals. Cell 124:901–914. doi:10.1016/j.cell.2006.02.024 PubMedCrossRefGoogle Scholar
  32. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162CrossRefGoogle Scholar
  33. Greve G, Alechine E, Pasantes JJ, Hodler C, Rietschel W, Robinson TJ, Schempp W (2011) Y-Chromosome variation in hominids: intraspecific variation is limited to the polygamous chimpanzee. PLoS One. doi:10.1371/journal.pone.0029311 Google Scholar
  34. Guschanski K, Caillaud D, Robbins MM, Vigilant L (2008) Females shape the genetic structure of a gorilla population. Curr Biol 18:1809–1814. doi:10.1016/j.cub.2008.10.031 PubMedCrossRefGoogle Scholar
  35. Hallast P, Balaresque P, Bowden GR, Ballereau S, Jobling MA (2013) Recombination dynamics of a human Y-chromosomal palindrome: rapid GC-biased gene conversion, multi-kilobase conversion tracts, and rare inversions. PLoS Genet 9:e1003666. doi:10.1371/journal.pgen.1003666 PubMedPubMedCentralCrossRefGoogle Scholar
  36. Hallast P, Batini C, Zadik D, Maisano Delser P, Wetton JH, Arroyo-Pardo E, Cavalleri GL, de Knijff P, Destro Bisol G, Dupuy BM, Eriksen HA, Jorde LB, King TE, Larmuseau MH, Lopez de Munain A, Lopez-Parra AM, Loutradis A, Milasin J, Novelletto A, Pamjav H, Sajantila A, Schempp W, Sears M, Tolun A, Tyler-Smith C, Van Geystelen A, Watkins S, Winney B, Jobling MA (2015) The Y-chromosome tree bursts into leaf: 13,000 high-confidence SNPs covering the majority of known clades. Mol Biol Evol 32:661–673. doi:10.1093/molbev/msu327 PubMedCrossRefGoogle Scholar
  37. Hallast P, Maisano Delser P, Batini C, Zadik D, Rocchi M, Schempp W, Tyler-Smith C, Jobling MA (2016) Great ape Y Chromosome and mitochondrial DNA phylogenies reflect subspecies structure and patterns of mating and dispersal. Genome Res 26:427–439. doi:10.1101/gr.198754.115 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Harcourt AH, Stewart KJ (2007) Gorilla society: what we know and don’t know. Evol Anthropol 16:147–158. doi:10.1002/evan.20142 CrossRefGoogle Scholar
  39. Hill KR, Walker RS, Bozicevic M, Eder J, Headland T, Hewlett B, Hurtado AM, Marlowe FW, Wiessner P, Wood B (2011) Co-residence patterns in hunter-gatherer societies show unique human social structure. Science 331:1286–1289. doi:10.1126/science.1199071 PubMedCrossRefGoogle Scholar
  40. Hohmann G (2001) Association and social interactions between strangers and residents in bonobos (Pan paniscus). Primates 42:91–99CrossRefGoogle Scholar
  41. Hughes JF, Rozen S (2012) Genomics and genetics of human and primate y chromosomes. Annu Rev Genomics Hum Genet 13:83–108. doi:10.1146/annurev-genom-090711-163855 PubMedCrossRefGoogle Scholar
  42. Hughes JF, Skaletsky H, Pyntikova T, Minx PJ, Graves T, Rozen S, Wilson RK, Page DC (2005) Conservation of Y-linked genes during human evolution revealed by comparative sequencing in chimpanzee. Nature 437:101–104. doi:10.1038/nature04101 Google Scholar
  43. Hughes JF, Skaletsky H, Pyntikova T, Graves TA, van Daalen SKM, Minx PJ, Fulton RS, McGrath SD, Locke DP, Friedman C, Trask BJ, Mardis ER, Warren WC, Repping S, Rozen S, Wilson RK, Page DC (2010) Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature 463:536–539. doi:10.1038/nature08700 PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hughes JF, Skaletsky H, Brown LG, Pyntikova T, Graves T, Fulton RS, Dugan S, Ding Y, Buhay CJ, Kremitzki C, Wang QY, Shen H, Holder M, Villasana D, Nazareth LV, Cree A, Courtney L, Veizer J, Kotkiewicz H, Cho TJ, Koutseva N, Rozen S, Muzny DM, Warren WC, Gibbs RA, Wilson RK, Page DC (2012) Strict evolutionary conservation followed rapid gene loss on human and rhesus Y chromosomes. Nature 483:U82–U124. doi:10.1038/nature10843 CrossRefGoogle Scholar
  45. Hvilsom C, Carlsen F, Heller R, Jaffre N, Siegismund HR (2014) Contrasting demographic histories of the neighboring bonobo and chimpanzee. Primates 55:101–112. doi:10.1007/s10329-013-0373-3 PubMedCrossRefGoogle Scholar
  46. Inoue E, Akomo-Okoue EF, Ando C, Iwata Y, Judai M, Fujita S, Hongo S, Nze-Nkogue C, Inoue-Murayama M, Yamagiwa J (2013) Male genetic structure and paternity in western lowland gorillas (Gorilla gorilla gorilla). Am J Phys Anthropol 151:583–588. doi:10.1002/ajpa.22312 PubMedCrossRefGoogle Scholar
  47. Jobling MA (2008) Copy number variation on the human Y chromosome. Cytogenet Genome Res 123:253–262. doi:10.1159/000184715 PubMedCrossRefGoogle Scholar
  48. Jobling MA, Lo IC, Turner DJ, Bowden GR, Lee AC, Xue Y, Carvalho-Silva D, Hurles ME, Adams SM, Chang YM, Kraaijenbrink T, Henke J, Guanti G, McKeown B, van Oorschot RA, Mitchell RJ, de Knijff P, Tyler-Smith C, Parkin EJ (2007) Structural variation on the short arm of the human Y chromosome: recurrent multigene deletions encompassing Amelogenin Y. Hum Mol Genet 16:307–316. doi:10.1093/hmg/ddl465 PubMedCrossRefGoogle Scholar
  49. Kirsch S, Munch C, Jiang ZS, Cheng Z, Chen L, Batz C, Eichler EE, Schempp W (2008) Evolutionary dynamics of segmental duplications from human Y-chromosomal euchromatin/heterochromatin transition regions. Genome Res 18:1030–1042. doi:10.1101/gr.076711.108 PubMedPubMedCentralCrossRefGoogle Scholar
  50. Knebel S, Pasantes JJ, Thi DAD, Schaller F, Schempp W (2011) Heterogeneity of pericentric inversions of the human Y chromosome. Cytogenet Genome Res 132:219–226. doi:10.1159/000322080 PubMedCrossRefGoogle Scholar
  51. Krausz C, Degl’Innocenti S, Nuti F, Morelli A, Felici F, Sansone M, Varriale G, Forti G (2006) Natural transmission of USP9Y gene mutations: a new perspective on the role of AZFa genes in male fertility. Hum Mol Genet 15:2673–2681. doi:10.1093/hmg.ddl198 PubMedCrossRefGoogle Scholar
  52. Kuroki Y, Toyoda A, Noguchi H, Taylor TD, Itoh T, Kim DS, Kim DW, Choi SH, Kim IC, Choi HH, Kim YS, Satta Y, Saitou N, Yamada T, Morishita S, Hattori M, Sakaki Y, Park HS, Fujiyama A (2006) Comparative analysis of chimpanzee and human Y chromosomes unveils complex evolutionary pathway Nat Genet 38:158– + doi:10.1038/ng1729
  53. Lahn BT, Page DC (1999) Four evolutionary strata on the human X chromosome. Science 286:964–967PubMedCrossRefGoogle Scholar
  54. Lange J, Skaletsky H, van Daalen SK, Embry SL, Korver CM, Brown LG, Oates RD, Silber S, Repping S, Page DC (2009) Isodicentric Y chromosomes and sex disorders as byproducts of homologous recombination that maintains palindromes. Cell 138:855–869. doi:10.1016/j.cell.2009.07.042 PubMedPubMedCentralCrossRefGoogle Scholar
  55. Lange J, Noordam MJ, van Daalen SKM, Skaletsky H, Clark BA, Macville MV, Page DC, Repping S (2013) Intrachromosomal homologous recombination between inverted amplicons on opposing Y-chromosome arms. Genomics 102:257–264. doi:10.1016/j.ygeno.2013.04.018 PubMedCrossRefGoogle Scholar
  56. Langergraber KE, Siedel H, Mitani JC, Wrangham RW, Reynolds V, Hunt K, Vigilant L (2007) The Genetic Signature of Sex-Biased Migration in Patrilocal Chimpanzees and Humans. PLoS One. doi:10.1371/journal.pone.0000973 PubMedPubMedCentralGoogle Scholar
  57. Langergraber KE, Rowney C, Schubert G, Crockford C, Hobaiter C, Wittig R, Wrangham RW, Zuberbuhler K, Vigilant L (2014) How old are chimpanzee communities? Time to the most recent common ancestor of the Y-chromosome in highly patrilocal societies J Hum Evol 69:1–7. doi:10.1016/j.jhevol.2013.12.005 PubMedGoogle Scholar
  58. Li G, Davis BW, Raudsepp T, Wilkerson AJP, 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 23:1486–1495. doi:10.1101/gr.154286.112 PubMedPubMedCentralCrossRefGoogle Scholar
  59. Livernois AM, Graves JAM, Waters PD (2012) The origin and evolution of vertebrate sex chromosomes and dosage compensation. Heredity 108:50–58. doi:10.1038/hdy.2011.106 PubMedCrossRefGoogle Scholar
  60. Lobon I, Tucci S, de Manuel M, Ghirotto S, Benazzo A, Prado-Martinez J, Lorente-Galdos B, Nam K, Dabad M, Hernandez-Rodriguez J, Comas D, Navarro A, Schierup MH, Andres AM, Barbujani G, Hvilsom C, Marques-Bonet T (2016) Demographic history of the genus pan inferred from whole mitochondrial genome reconstructions. Genome Biol Evol 8:2020–2030. doi:10.1093/gbe/evw124 PubMedPubMedCentralCrossRefGoogle Scholar
  61. Locke DP, Hillier LW, Warren WC, Worley KC, Nazareth LV, Muzny DM, Yang SP, Wang Z, Chinwalla AT, Minx P, Mitreva M, Cook L, Delehaunty KD, Fronick C, Schmidt H, Fulton LA, Fulton RS, Nelson JO, Magrini V, Pohl C, Graves TA, Markovic C, Cree A, Dinh HH, Hume J, Kovar CL, Fowler GR, Lunter G, Meader S, Heger A, Ponting CP, Marques-Bonet T, Alkan C, Chen L, Cheng Z, Kidd JM, Eichler EE, White S, Searle S, Vilella AJ, Chen Y, Flicek P, Ma J, Raney B, Suh B, Burhans R, Herrero J, Haussler D, Faria R, Fernando O, Darre F, Farre D, Gazave E, Oliva M, Navarro A, Roberto R, Capozzi O, Archidiacono N, Della Valle G, Purgato S, Rocchi M, Konkel MK, Walker JA, Ullmer B, Batzer MA, Smit AF, Hubley R, Casola C, Schrider DR, Hahn MW, Quesada V, Puente XS, Ordonez GR, Lopez-Otin C, Vinar T, Brejova B, Ratan A, Harris RS, Miller W, Kosiol C, Lawson HA, Taliwal V, Martins AL, Siepel A, Roychoudhury A, Ma X, Degenhardt J, Bustamante CD, Gutenkunst RN, Mailund T, Dutheil JY, Hobolth A, Schierup MH, Ryder OA, Yoshinaga Y, de Jong PJ, Weinstock GM, Rogers J, Mardis ER, Gibbs RA, Wilson RK (2011) Comparative and demographic analysis of orang-utan genomes. Nature 469:529–533. doi:10.1038/nature09687 PubMedPubMedCentralCrossRefGoogle Scholar
  62. Luddi A, Margollicci M, Gambera L, Serafini F, Cioni M, De Leo V, Balestri P, Piomboni P (2009) Brief report: spermatogenesis in a man with complete deletion of USP9Y. New Engl J Med 360:881–885. doi:10.1056/NEJMoa0806218 PubMedCrossRefGoogle Scholar
  63. Ma X, Kelley JL, Eilertson K, Musharoff S, Degenhardt JD, Martins AL, Vinar T, Kosiol C, Siepel A, Gutenkunst RN, Bustamante CD (2013) Population genomic analysis reveals a rich speciation and demographic history of orangutans (Pongo pygmaeus and Pongo abelii). PLoS One. doi:10.1371/journal.pone.0077175 Google Scholar
  64. Marais GA, Campos PR, Gordo I (2010) Can intra-Y gene conversion oppose the degeneration of the human Y chromosome? A simulation study. Genome Biol Evol 2:347–357. doi:10.1093/gbe/evq026 PubMedPubMedCentralCrossRefGoogle Scholar
  65. Marvan R, Stevens JM, Roeder AD, Mazura I, Bruford MW, de Ruiter JR (2006) Male dominance rank, mating and reproductive success in captive bonobos (Pan paniscus) Folia Primatol (Basel) 77:364–376 doi:10.1159/000093702
  66. Mendez FL, Poznik GD, Castellano S, Bustamantel CD (2016) The divergence of neandertal and modern human Y chromosomes. Am J Hum Genet 98:728–734. doi:10.1016/j.ajhg.2016.02.023 PubMedPubMedCentralCrossRefGoogle Scholar
  67. Mendez-Lago M, Bergman CM, de Pablos B, Tracey A, Whitehead SL, Villasante A (2011) A large palindrome with interchromosomal gene duplications in the pericentromeric region of the D. melanogaster Y chromosome. Mol Biol Evol 28:1967–1971PubMedPubMedCentralCrossRefGoogle Scholar
  68. Murphy KM, Cohen JS, Goodrich A, Long PP, Griffin CA (2007) Consultations in molecular diagnostics: constitutional duplication of a region of chromosome Yp encoding AMELY, PRKY, and TBL1Y: Implications for sex chromosome analysis and bone marrow engraftment analysis. J Mol Diagn 9:408–413. doi:10.2353/jmoldx.2007.060198 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Murtagh VJ, O’Meally D, Sankovic N, Delbridge ML, Kuroki Y, Boore JL, Toyoda A, Jordan KS, Pask AJ, Renfree MB, Fujiyama A, Graves JAM, Waters PD (2012) Evolutionary history of novel genes on the tammar wallaby Y chromosome: implications for sex chromosome evolution. Genome Res 22:498–507PubMedPubMedCentralCrossRefGoogle Scholar
  70. Nater A, Nietlisbach P, Arora N, van Schaik CP, van Noordwijk MA, Willems EP, Singleton I, Wich SA, Goossens B, Warren KS, Verschoor EJ, Perwitasari-Farajallah D, Pamungkas J, Krutzen M (2011) Sex-biased dispersal and volcanic activities shaped phylogeographic patterns of extant orangutans (genus: Pongo). Mol Biol Evol 28:2275–2288. doi:10.1093/molbev/msr042 PubMedCrossRefGoogle Scholar
  71. Nater A, Arora N, Greminger MP, van Schaik CP, Singleton I, Wich SA, Fredriksson G, Perwitasari-Farajallah D, Pamungkas J, Krutzen M (2013) Marked population structure and recent migration in the critically endangered sumatran orangutan (Pongo abelii) J Hered 104:2. doi:10.1093/jhered/ess065
  72. Nietlisbach P, Nater A, Greminger MP, Arora N, Krutzen M (2010) A multiplex-system to target 16 male-specific and 15 autosomal genetic markers for orang-utans (genus: Pongo) Conserv Genet Resour 2:153–158Google Scholar
  73. Nietlisbach P, Arora N, Nater A, Goossens B, van Schaik CP, Krutzen M (2012) Heavily male-biased long-distance dispersal of orangutans (genus: Pongo), as revealed by Y-chromosomal and mitochondrial genetic markers. Mol Ecol 21:3173–3186. doi:10.1111/j.1365-294X.2012.05539.x PubMedCrossRefGoogle Scholar
  74. Nishida T, Corp N, Hamai M, Hasegawa T, Hiraiwa-Hasegawa M, Hosaka K, Hunt KD, Itoh N, Kawanaka K, Matsumoto-Oda A, Mitani JC, Nakamura M, Norikoshi K, Sakamaki T, Turner L, Uehara S, Zamma K (2003) Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. Am J Primatol 59:99–121PubMedCrossRefGoogle Scholar
  75. Oetjens MT, Shen FC, Emery SB, Zou ZT, Kidd JM (2016) Y-chromosome structural diversity in the bonobo and chimpanzee lineages. Genome Biol Evol 8:2231–2240. doi:10.1093/gbe/evw150 PubMedPubMedCentralCrossRefGoogle Scholar
  76. Ohno S (1967) Conservation of the original X and homology of the X linked genes in placental mammals. Sex chromosomes and sex-linked genes: monographs on endocrinology. Springer, Berlin/Heidelberg, pp 46–73CrossRefGoogle Scholar
  77. Paria N, Raudsepp T, Wilkerson AJP, O’Brien PCM, Ferguson-Smith MA, Love CC, Arnold C, Rakestraw P, Murphy WJ, Chowdhary BP (2011) A gene catalogue of the euchromatic male-specific region of the horse Y chromosome: comparison with human and other mammals. PLoS One. doi:10.1371/journal.pone.0021374 PubMedPubMedCentralGoogle Scholar
  78. Perry GH, Tito RY, Verrelli BC (2007) The evolutionary history of human and chimpanzee Y-chromosome gene loss. Mol Biol Evol 24:853–859. doi:10.1093/molbev/msm002 PubMedCrossRefGoogle Scholar
  79. Poznik GD, Xue Y, Mendez FL, Willems TF, Massaia A, Wilson Sayres MA, Ayub Q, McCarthy SA, Narechania A, Kashin S, Chen Y, Banerjee R, Rodriguez-Flores JL, Cerezo M, Shao H, Gymrek M, Malhotra A, Louzada S, Desalle R, Ritchie GR, Cerveira E, Fitzgerald TW, Garrison E, Marcketta A, Mittelman D, Romanovitch M, Zhang C, Zheng-Bradley X, Abecasis GR, McCarroll SA, Flicek P, Underhill PA, Coin L, Zerbino DR, Yang F, Lee C, Clarke L, Auton A, Erlich Y, Handsaker RE, Genomes Project C, Bustamante CD, Tyler-Smith C (2016) Punctuated bursts in human male demography inferred from 1244 worldwide Y-chromosome sequences. Nat Genet 48:593–599. doi:10.1038/ng.3559 PubMedPubMedCentralCrossRefGoogle Scholar
  80. Prado-Martinez J, Sudmant PH, Kidd JM, Li H, Kelley JL, Lorente-Galdos B, Veeramah KR, Woerner AE, O’Connor TD, Santpere G, Cagan A, Theunert C, Casals F, Laayouni H, Munch K, Hobolth A, Halager AE, Malig M, Hernandez-Rodriguez J, Hernando-Herraez I, Prufer K, Pybus M, Johnstone L, Lachmann M, Alkan C, Twigg D, Petit N, Baker C, Hormozdiari F, Fernandez-Callejo M, Dabad M, Wilson ML, Stevison L, Camprubi C, Carvalho T, Ruiz-Herrera A, Vives L, Mele M, Abello T, Kondova I, Bontrop RE, Pusey A, Lankester F, Kiyang JA, Bergl RA, Lonsdorf E, Myers S, Ventura M, Gagneux P, Comas D, Siegismund H, Blanc J, Agueda-Calpena L, Gut M, Fulton L, Tishkoff SA, Mullikin JC, Wilson RK, Gut IG, Gonder MK, Ryder OA, Hahn BH, Navarro A, Akey JM, Bertranpetit J, Reich D, Mailund T, Schierup MH, Hvilsom C, Andres AM, Wall JD, Bustamante CD, Hammer MF, Eichler EE, Marques-Bonet T (2013) Great ape genetic diversity and population history. Nature 499:471–475. doi:10.1038/nature12228 PubMedPubMedCentralCrossRefGoogle Scholar
  81. Prufer K, Munch K, Hellmann I, Akagi K, Miller JR, Walenz B, Koren S, Sutton G, Kodira C, Winer R, Knight JR, Mullikin JC, Meader SJ, Ponting CP, Lunter G, Higashino S, Hobolth A, Dutheil J, Karakoc E, Alkan C, Sajjadian S, Catacchio CR, Ventura M, Marques-Bonet T, Eichler EE, Andre C, Atencia R, Mugisha L, Junhold J, Patterson N, Siebauer M, Good JM, Fischer A, Ptak SE, Lachmann M, Symer DE, Mailund T, Schierup MH, Andres AM, Kelso J, Paabo S (2012) The bonobo genome compared with the chimpanzee and human genomes. Nature 486:527–531. doi:10.1038/nature11128 PubMedPubMedCentralGoogle Scholar
  82. Repping S, van Daalen SK, Brown LG, Korver CM, Lange J, Marszalek JD, Pyntikova T, van der Veen F, Skaletsky H, Page DC, Rozen S (2006) High mutation rates have driven extensive structural polymorphism among human Y chromosomes. Nat Genet 38:463–467. doi:10.1038/ng1754 PubMedCrossRefGoogle Scholar
  83. Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, Muzny D, Platzer M, Howell GR, Burrows C, Bird CP, Frankish A, Lovell FL, Howe KL, Ashurst JL, Fulton RS, Sudbrak R, Wen GP, Jones MC, Hurles ME, Andrews TD, Scott CE, Searle S, Ramser J, Whittaker A, Deadman R, Carter NP, Hunt SE, Chen R, Cree A, Gunaratne P, Havlak P, Hodgson A, Metzker ML, Richards S, Scott G, Steffen D, Sodergren E, Wheeler DA, Worley KC, Ainscough R, Ambrose KD, Ansari-Lari MA, Aradhya S, Ashwell RIS, Babbage AK, Bagguley CL, Ballabio A, Banerjee R, Barker GE, Barlow KF, Barrett IP, Bates KN, Beare DM, Beasley H, Beasley O, Beck A, Bethel G, Blechschmidt K, Brady N, Bray-Allen S, Bridgeman AM, Brown AJ, Brown MJ, Bonnin D, Bruford EA, Buhay C, Burch P, Burford D, Burgess J, Burrill W, Burton J, Bye JM, Carder C, Carrel L, Chako J, Chapman JC, Chavez D, Chen E, Chen G, Chen Y, Chen ZJ, Chinault C, Ciccodicola A, Clark SY, Clarke G, Clee CM, Clegg S, Clerc-Blankenburg K, Clifford K, Cobley V, Cole CG, Conquer JS, Corby N, Connor RE, David R, Davies J, Davis C, Davis J, Delgado O, DeShazo D, Dhami P, Ding Y, Dinh H, Dodsworth S, Draper H, Dugan-Rocha S, Dunham A, Dunn M, Durbin KJ, Dutta I, Eades T, Ellwood M, Emery-Cohen A, Errington H, Evans KL, Faulkner L, Francis F, Frankland J, Fraser AE, Galgoczy P, Gilbert J, Gill R, Glockner G, Gregory SG, Gribble S, Griffiths C, Grocock R, Gu YH, Gwilliam R, Hamilton C, Hart EA, Hawes A, Heath PD, Heitmann K, Hennig S, Hernandez J, Hinzmann B, Ho S, Hoffs M, Howden PJ, Huckle EJ, Hume J, Hunt PJ, Hunt AR, Isherwood J, Jacob L, Johnson D, Jones S, de Jong PJ, Joseph SS, Keenan S, Kelly S, Kershaw JK, Khan Z, Kioschis P, Klages S, Knights AJ, Kosiura A, Kovar-Smith C, Laird GK, Langford C, Lawlor S, Leversha M, Lewis L, Liu W, Lloyd C, Lloyd DM, Loulseged H, Loveland JE, Lovell JD, Lozado R, Lu J, Lyne R, Ma J, Maheshwari M, Matthews LH, McDowall J, McLaren S, McMurray A, Meidl P, Meitinger T, Milne S, Miner G, Mistry SL, Morgan M, Morris S, Muller I, Mullikin JC, Nguyen N, Nordsiek G, Nyakatura G, O’Dell CN, Okwuonu G, Palmer S, Pandian R, Parker D, Parrish J, Pasternak S, Patel D, Pearce AV, Pearson DM, Pelan SE, Perez L, Porter KM, Ramsey Y, Reichwald K, Rhodes S, Ridler KA, Schlessinger D, Schueler MG, Sehra HK, Shaw-Smith C, Shen H, Sheridan EM, Shownkeen R, Skuce CD, Smith ML, Sotheran EC, Steingruber HE, Steward CA, Storey R, Swann RM, Swarbreck D, Tabor PE, Taudien S, Taylor T, Teague B, Thomas K, Thorpe A, Timms K, Tracey A, Trevanion S, Tromans AC, d’Urso M, Verduzco D, Villasana D, Waldron L, Wall M, Wang QY, Warren J, Warry GL, Wei XH, West A, Whitehead SL, Whiteley MN, Wilkinson JE, Willey DL, Williams G, Williams L, Williamson A, Williamson H, Wilming L, Woodmansey RL, Wray PW, Yen J, Zhang JK, Zhou JL, Zoghbi H, Zorilla S, Buck D, Reinhardt R, Poustka A, Rosenthal A, Lehrach H, Meindl A, Minx PJ, Hillier LW, Willard HF, Wilson RK, Waterston RH, Rice CM, Vaudin M, Coulson A, Nelson DL, Weinstock G, Sulston JE, Durbin R, Hubbard T, Gibbs RA, Beck S, Rogers J, Bentley DR (2005) The DNA sequence of the human X chromosome. Nature 434:325–337. doi:10.1038/nature03440 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Rosser ZH, Balaresque P, Jobling MA (2009) Gene conversion between the X chromosome and the male-specific region of the Y chromosome at a translocation hotspot. Am J Hum Genet 85:130–134. doi:10.1016/j.ajhg.2009.06.009 PubMedPubMedCentralCrossRefGoogle Scholar
  85. Rozen S, Skaletsky H, Marszalek JD, Minx PJ, Cordum HS, Waterston RH, Wilson RK, Page DC (2003) Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 423:873–876. doi:10.1038/nature01723 PubMedCrossRefGoogle Scholar
  86. Rozen S, Marszalek JD, Alagappan RK, Skaletsky H, Page DC (2009) Remarkably little variation in proteins encoded by the Y chromosome’s single-copy genes, implying effective purifying selection. Am J Hum Genet 85:923–928. doi:10.1016/j.ajhg.2009.11.011 PubMedPubMedCentralCrossRefGoogle Scholar
  87. Santos FR, Pandya A, Tyler-Smith C (1998) Reliability of DNA-based sex tests Nat Genet 18:103. doi:10.1038/ng0298-103 PubMedGoogle Scholar
  88. Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I, Herrero J, Hobolth A, Lappalainen T, Mailund T, Marques-Bonet T, McCarthy S, Montgomery SH, Schwalie PC, Tang YA, Ward MC, Xue Y, Yngvadottir B, Alkan C, Andersen LN, Ayub Q, Ball EV, Beal K, Bradley BJ, Chen Y, Clee CM, Fitzgerald S, Graves TA, Gu Y, Heath P, Heger A, Karakoc E, Kolb-Kokocinski A, Laird GK, Lunter G, Meader S, Mort M, Mullikin JC, Munch K, O’Connor TD, Phillips AD, Prado-Martinez J, Rogers AS, Sajjadian S, Schmidt D, Shaw K, Simpson JT, Stenson PD, Turner DJ, Vigilant L, Vilella AJ, Whitener W, Zhu B, Cooper DN, de Jong P, Dermitzakis ET, Eichler EE, Flicek P, Goldman N, Mundy NI, Ning Z, Odom DT, Ponting CP, Quail MA, Ryder OA, Searle SM, Warren WC, Wilson RK, Schierup MH, Rogers J, Tyler-Smith C, Durbin R (2012) Insights into hominid evolution from the gorilla genome sequence. Nature 483:169–175. doi:10.1038/nature10842 PubMedPubMedCentralCrossRefGoogle Scholar
  89. Schaller F, Fernandes AM, Hodler C, Munch C, Pasantes JJ, Rietschel W, Schempp W (2010) Y chromosomal variation tracks the evolution of mating systems in chimpanzee and bonobo. PLoS One. doi:10.1371/journal.pone.0012482 Google Scholar
  90. Schempp W, Toder R, Rietschel W, Grutzner F, Mayerova A, Gauckler A (1993) Inverted and satellited Y chromosome in the orangutan (Pongo pygmaeus). Chromosome Res 1:69–75PubMedCrossRefGoogle Scholar
  91. Schempp W, Binkele A, Arnemann J, Glaser B, Ma K, Taylor K, Toder R, Wolfe J, Zeitler S, Chandley AC (1995) Comparative mapping of yrrm-related and tspy-related cosmids in man and hominoid apes. Chromosome Res 3:227–234PubMedCrossRefGoogle Scholar
  92. Schmid M, Haaf T, Solleder E, Schempp W, Leipoldt M, Heilbronner H (1984) Satellited Y chromosomes: structure, origin, and clinical significance. Hum Genet 67:72–85PubMedCrossRefGoogle Scholar
  93. Schmidt J, Kirsch S, Rappold GA, Schempp W (2009) Complex evolution of a Y-chromosomal double homeobox 4 (DUX4)-related gene family in hominoids. PLoS One 4:e5288. doi:10.1371/journal.pone.0005288 PubMedPubMedCentralCrossRefGoogle Scholar
  94. Schubert G, Stoneking CJ, Arandjelovic M, Boesch C, Eckhardt N, Hohmann G, Langergraber K, Lukas D, Vigilant L (2011) Male-mediated gene flow in patrilocal primates. PLoS One. doi:10.1371/journal.pone.0021514 Google Scholar
  95. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova T, Ali J, Bieri T, Chinwalla A, Delehaunty A, Delehaunty K, Du H, Fewell G, Fulton L, Fulton R, Graves T, Hou SF, Latrielle P, Leonard S, Mardis E, Maupin R, McPherson J, Miner T, Nash W, Nguyen C, Ozersky P, Pepin K, Rock S, Rohlfing T, Scott K, Schultz B, Strong C, Tin-Wollam A, Yang SP, Waterston RH, Wilson RK, Rozen S, Page DC (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:U822–U825CrossRefGoogle Scholar
  96. Skinner BM, Sargent CA, Churcher C, Hunt T, Herrero J, Loveland JE, Dunn M, Louzada S, Fu BY, Chow W, Gilbert J, Austin-Guest S, Beal K, Carvalho-Silva D, Cheng W, Gordon D, Grafham D, Hardy M, Harley J, Hauser H, Howden P, Howe K, Lachani K, Ellis PJI, Kelly D, Kerry G, Kerwin J, Ng BL, Threadgold G, Wileman T, Wood JMD, Yang FT, Harrow J, Affara NA, Tyler-Smith C (2016) The pig X and Y chromosomes: structure, sequence, and evolution. Genome Res 26:130–139PubMedPubMedCentralCrossRefGoogle Scholar
  97. Soh YQS, Alfoldi J, Pyntikova T, Brown LG, Graves T, Minx PJ, Fulton RS, Kremitzki C, Koutseva N, Mueller JL, Rozen S, Hughes JF, Owens E, Womack JE, Murphy WJ, Cao Q, de Jong P, Warren WC, Wilson RK, Skaletsky H, Page DC (2014) Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes. Cell 159:800–813PubMedPubMedCentralCrossRefGoogle Scholar
  98. Stone AC, Griffiths RC, Zegura SL, Hammer MF (2002) High levels of Y-chromosome nucleotide diversity in the genus Pan P. Natl Acad Sci USA 99:43–48 doi: 10.1073/pnas.012364999
  99. Sun C, Sklaetsky H, Birren B, Devon K, Tang ZL, Silber S, Oates R, Page DC (1999) An azoospermic man with a de novo point mutation in the Y-chromosomal gene USP9Y. Nat Genet 23:429–432PubMedCrossRefGoogle Scholar
  100. Toder R, Zeitler S, Goodfellow PN, Schempp W (1993) Comparative mapping of SRY in the great apes. Chromosome Res 1:117–120PubMedCrossRefGoogle Scholar
  101. Tomaszkiewicz M, Rangavittal S, Cechova M, Sanchez RC, Fescemyer HW, Harris R, Ye DL, O’Brien PCM, Chikhi R, Ryder OA, Ferguson-Smith MA, Medvedev P, Makova KD (2016) A time- and cost-effective strategy to sequence mammalian Y Chromosomes: an application to the de novo assembly of gorilla Y. Genome Res 26:530–540PubMedPubMedCentralCrossRefGoogle Scholar
  102. Treangen TJ, Salzberg SL (2011) Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet 13:36–46. doi:10.1038/nrg3117 PubMedPubMedCentralGoogle Scholar
  103. Trombetta B, Cruciani F, Underhill PA, Sellitto D, Scozzari R (2010) Footprints of X-to-Y gene conversion in recent human evolution. Mol Biol Evol 27:714–725. doi:10.1093/molbev/msp231 PubMedCrossRefGoogle Scholar
  104. Trombetta B, Sellitto D, Scozzari R, Cruciani F (2014) Inter- and intraspecies phylogenetic analyses reveal extensive X-Y gene conversion in the evolution of gametologous sequences of human sex chromosomes. Mol Biol Evol 31:2108–2123. doi:10.1093/molbev/msu155 PubMedPubMedCentralCrossRefGoogle Scholar
  105. Trombetta B, Fantini G, D’Atanasio E, Sellitto D, Cruciani F (2016) Evidence of extensive non-allelic gene conversion among LTR elements in the human genome. Sci Rep 6:28710. doi:10.1038/srep28710 PubMedPubMedCentralCrossRefGoogle Scholar
  106. Vallender EJ, Lahn BT (2004) Effects of chromosomal rearrangements on human-chimpanzee molecular evolution. Genomics 84:757–761PubMedCrossRefGoogle Scholar
  107. Verma RS, Dosik H, Scharf T, Lubs HA (1978) Length heteromorphisms of fluorescent (f) and non-fluorescent (nf) segments of human Y chromosome: classification, frequencies, and incidence in normal Caucasians. J Med Genet 15:277–281PubMedPubMedCentralCrossRefGoogle Scholar
  108. Verma RS, Rodriguez J, Dosik H (1982) The clinical significance of pericentric inversion of the human Y chromosome: a rare “third” type of heteromorphism. J Hered 73:236–238PubMedCrossRefGoogle Scholar
  109. Vervaecke H, Vanelsacker L (1992) Hybrids between common chimpanzees (Pan-Troglodytes) and pygmy chimpanzees (Pan-Paniscus) in captivity. Mammalia 56:667–669Google Scholar
  110. Vogt PH, Edelmann A, Kirsch S, Henegariu O, Hirschmann P, Kiesewetter F, Kohn FM, Schill WB, Farah S, Ramos C, Hartmann M, Hartschuh W, Meschede D, Behre HM, Castel A, Nieschlag E, Weidner W, Grone HJ, Jung A, Engel W, Haidl G (1996) Human Y chromosome azoospermia factors (AZF) mapped to different subregions in Yq11. Hum Mol Genet 5:933–943PubMedCrossRefGoogle Scholar
  111. Vollrath D, Foote S, Hilton A, Brown LG, Beer-Romero P, Bogan JS, Page DC (1992) The human Y chromosome: a 43-interval map based on naturally occurring deletions. Science 258:52–59PubMedCrossRefGoogle Scholar
  112. Weber B, Schempp W, Wiesner H (1986) An evolutionarily conserved early replicating segment on the sex-chromosomes of man and the great apes cytogenet cell genet 43:72–78Google Scholar
  113. Wei W, Ayub Q, Chen Y, McCarthy S, Hou Y, Carbone I, Xue Y, Tyler-Smith C (2013a) A calibrated human Y-chromosomal phylogeny based on resequencing. Genome Res 23:388–395. doi:10.1101/gr.143198.112 PubMedPubMedCentralCrossRefGoogle Scholar
  114. Wei W, Ayub Q, Xue YL, Tyler-Smith C (2013b) A comparison of Y-chromosomal lineage dating using either resequencing or Y-SNP plus Y-STR genotyping Forensic Sci Int-Gen 7:568–572. doi:10.1016/j.fsigen.2013.03.014 PubMedPubMedCentralGoogle Scholar
  115. Wei W, Fitzgerald TW, Ayub Q, Massaia A, Smith BH, Dominiczak AF, Morris AD, Porteous DJ, Hurles ME, Tyler-Smith C, Xue Y (2015) Copy number variation in the human Y chromosome in the UK population. Hum Genet 134:789–800. doi:10.1007/s00439-015-1562-5 PubMedPubMedCentralCrossRefGoogle Scholar
  116. Willems T, Gymrek M, Poznik GD, Tyler-Smith C, Genomes Project Chromosome YG, Erlich Y (2016) Population-scale sequencing data enable precise estimates of Y-STR mutation rates. Am J Hum Genet 98:919–933. doi:10.1016/j.ajhg.2016.04.001 PubMedPubMedCentralCrossRefGoogle Scholar
  117. Xue Y, Tyler-Smith C (2011) An exceptional gene: evolution of the TSPY gene family in humans and other great apes genes (Basel) 2:36–47. doi:10.3390/genes2010036 Google Scholar
  118. Xue YL, Prado-Martinez J, Sudmant PH, Narasimhan V, Ayub Q, Szpak M, Frandsen P, Chen Y, Yngvadottir B, Cooper DN, de Manuel M, Hernandez-Rodriguez J, Lobon I, Siegismund HR, Pagani L, Quail MA, Hvilsom C, Mudakikwa A, Eichler EE, Cranfield MR, Marques-Bonet T, Tyler-Smith C, Scally A (2015) Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding. Science 348:242–245. doi:10.1126/science.aaa3952 PubMedPubMedCentralCrossRefGoogle Scholar
  119. Yu YH, Lin YW, Yu JF, Schempp W, Yen PH (2008) Evolution of the DAZ gene and the AZFc region on primate Y chromosomes. BMC Evol Biol 8:96. doi:10.1186/1471-2148-8-96 PubMedPubMedCentralCrossRefGoogle Scholar
  120. Yunis JJ, Prakash O (1982) The origin of man: a chromosomal pictorial legacy. Science 215:1525–1530PubMedCrossRefGoogle Scholar
  121. Zheng GX, Lau BT, Schnall-Levin M, Jarosz M, Bell JM, Hindson CM, Kyriazopoulou-Panagiotopoulou S, Masquelier DA, Merrill L, Terry JM, Mudivarti PA, Wyatt PW, Bharadwaj R, Makarewicz AJ, Li Y, Belgrader P, Price AD, Lowe AJ, Marks P, Vurens GM, Hardenbol P, Montesclaros L, Luo M, Greenfield L, Wong A, Birch DE, Short SW, Bjornson KP, Patel P, Hopmans ES, Wood C, Kaur S, Lockwood GK, Stafford D, Delaney JP, Wu I, Ordonez HS, Grimes SM, Greer S, Lee JY, Belhocine K, Giorda KM, Heaton WH, McDermott GP, Bent ZW, Meschi F, Kondov NO, Wilson R, Bernate JA, Gauby S, Kindwall A, Bermejo C, Fehr AN, Chan A, Saxonov S, Ness KD, Hindson BJ, Ji HP (2016) Haplotyping germline and cancer genomes with high-throughput linked-read sequencing. Nat Biotechnol 34:303–311. doi:10.1038/nbt.3432 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Institute of Molecular and Cell BiologyUniversity of TartuTartuEstonia
  2. 2.Wellcome Trust Sanger InstituteHinxtonUK
  3. 3.Department of GeneticsUniversity of LeicesterLeicesterUK

Personalised recommendations