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Dynamics of vertebrate sex chromosome evolution: from equal size to giants and dwarfs

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Abstract

The Y and W chromosomes of mammals and birds are known to be small because most of their genetic content degenerated and were lost due to absence of recombination with the X or Z, respectively. Thus, a picture has emerged of ever-shrinking Ys and Ws that may finally even fade into disappearance. We review here the large amount of literature on sex chromosomes in vertebrate species and find by taking a closer look, particularly at the sex chromosomes of fishes, amphibians and reptiles where several groups have evolutionary younger chromosomes than those of mammals and birds, that the perception of sex chromosomes being doomed to size reduction is incomplete. Here, sex-determining mechanisms show a high turnover and new sex chromosomes appear repeatedly. In many species, Ys and Ws are larger than their X and Z counterparts. This brings up intriguing perspectives regarding the evolutionary dynamics of sex chromosomes. It can be concluded that, due to accumulation of repetitive DNA and transposons, the Y and W chromosomes can increase in size during the initial phase of their differentiation.

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References

  • Aida T (1921) On the inheritance of color in a fresh-water fish, Aplocheilus latipes Temmick and Schlegel, with special reference to sex-linked inheritance. Genetics 6:554–573

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ananias F, Modesto ADS, Mendes SC, Napoli MF (2007) Unusual primitive heteromorphic ZZ/ZW sex chromosomes in Proceratophrys boiei (Anura, Cycloramphidae, Alsodinae), with description of C-band interpopulational polymorphism. Hereditas 144:206–212

    Article  PubMed  Google Scholar 

  • Ando K, Tagawa T, Uchida TA (1980) The C-banding pattern of 6 Japanese species of Vespertilionine bats (Mammalia, Chiroptera). Experientia 36:653–654

    Article  Google Scholar 

  • Andreata AA, de Almeida-Toledo LF, Oliveira C, de Almeida Toledo Filho S (1992) Chromosome studies in Hypoptopomatinae (Pisces, Siluriformes, Loricariidae) I. XX/XY Sex chromosome heteromorphism in Pseudotocinclus tietensis. Cytologia 57:369–372

    Article  Google Scholar 

  • Arslan A, Albayrak I, Pamukoglu N, Yorulmaz T, Toyran K (2009) C-banded karyotype and NORs of the long-eared hedgehog, Hemiechinus auritus from Turkey. Folia Zoologica 58:9–13

    Article  Google Scholar 

  • Artoni RF, Falcão JN, Moreira-Filho O, Bertollo LA (2001) An uncommon condition for a sex chromosome system in Characidae fish. Distribution and differentiation of the ZZ/ZW system in Triportheus. Chromosome Res 9:449–456

    Article  CAS  PubMed  Google Scholar 

  • Azevedo NF, Svartman M, Manchester A, de Moraes-Barros N, Stanyon R, Vianna-Morgante AM (2012) Chromosome painting in three-toed sloths: a cytogenetic signature and ancestral karyotype for Xenarthra. BMC Evol Biol 12:36

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badenhorst D, Stanyon R, Engstrom T, Valenzuela N (2013) A ZZ/ZW microchromosome system in the spiny softshell turtle, Apalone spinifera, reveals an intriguing sex chromosome conservation in Trionychidae. Chromosome Res 21:137–147

    Article  CAS  PubMed  Google Scholar 

  • Baroiller JF, D’Cotta H, Saillant E (2009) Environmental effects on fish sex determination and differentiation. Sex Dev 3:118–135

    Article  CAS  PubMed  Google Scholar 

  • Becak W, Becak ML, Nazareth HR, Ohno S (1964) Close karyological kinship between the reptilian suborder Serpentes and the class Aves. Chromosoma 15:606–617

    Article  CAS  PubMed  Google Scholar 

  • Bed’Hom B, Coullin P, Guillier-Gencik Z, Moulin S, Bernheim A, Volobouev V (2003) Characterization of the atypical karyotype of the black-winged kite Elanus caeruleus (Falconiformes: Accipitridae) by means of classical and molecular cytogenetic techniques. Chromosome Res 11:335–343

    Article  PubMed  Google Scholar 

  • Bellafronte E, Vicari MR, Artoni RF, Margarido VP, Moreira-Filho O (2009) Differentiated ZZ/ZW sex chromosomes in Apareiodon ibitiensis (Teleostei, Parodontidae): cytotaxonomy and biogeography. J Fish Biol 75:2313–2325

    Article  CAS  PubMed  Google Scholar 

  • Bellafronte E, Schemberger MO, Artoni RF, Filho OM, Vicari MR (2012) Sex chromosome system ZZ/ZW in Apareiodon hasemani Eigenmann, 1916 (Characiformes, Parodontidae) and a derived chromosomal region. Genet Mol Biol 35:770–776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergero R, Charlesworth D (2009) The evolution of restricted recombination in sex chromosomes. Trends Ecol Evol 24:94–102

    Article  PubMed  Google Scholar 

  • Bewick AJ, Chain FJ, Zimmerman LB, Sesay A, Gilchrist MJ, Owens ND, Seifertova E, Krylov V, Macha J, Tlapakova T, Kubickova S, Cernohorska H, Zarsky V, Evans BJ (2013) A large pseudoautosomal region on the sex chromosomes of the frog Silurana tropicalis. Genome Biol Evol 5:1087–1098

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Böhne A, Schultheis C, Galiana-Arnoux D, Froschauer A, Zhou Q, Schmidt C, Selz Y, Ozouf-Costaz C, Dettai A, Segurens B, Couloux A, Bernard-Samain S, Barbe V, Chilmonczyk S, Brunet F, Darras A, Tomaszkiewicz M, Semon M, Schartl M, Volff JN (2009) Molecular analysis of the sex chromosomes of the platyfish Xiphophorus maculatus: towards the identification of a new type of master sexual regulator in vertebrates. Integr Zool 4:277–284

    Article  PubMed  Google Scholar 

  • Borodin PM, Sablina OV, Rodionova MI (1995) Pattern of X-Y chromosome pairing in microtine rodents. Hereditas 123:17–23

    Article  CAS  PubMed  Google Scholar 

  • Busin CS, Andrade GV, Bertoldo J, Del Grande ML, Uetanabaro M, Recco-Pimentel SM (2008) Cytogenetic analysis of four species of Pseudis (Anura, Hylidae), with the description of ZZ/ZW sex chromosomes in P. tocantins. Genetica 133:119–127

    Article  PubMed  Google Scholar 

  • Cao X, Jiang H, Zhang X (2005) Polymorphic karyotypes and sex chromosomes in the tufted deer (Elaphodus cephalophus): cytogenetic studies and analyses of sex chromosome-linked genes. Cytogenet Genome Res 109:512–518

    Article  CAS  PubMed  Google Scholar 

  • Caparroz R, Duarte Barbanti JM (2004) Chromosomal similarity between the scaly-headed parrot (Pionus maximiliani), the short-tailed parrot (Graydidascalus brachyurus) and the yellow-faced parrot (Salvatoria xanthops) (Psittaciformes: Aves): a cytotaxonomic analysis. Genet Mol Biol 27:522–528

    Article  Google Scholar 

  • Centofante L, Carlos BLA, Moreira Filho O (2002) A ZZ/ZW sex chromosome system in a new species of the genus Parodon (Pisces, Parodontidae). Caryologia 55:139–150

    Article  Google Scholar 

  • Chalopin D, Volff JN, Galiana-Arnoux D, Anderson J, Schartl M (2015) Transposable elements and early evolution of sex chromosomes in fish. Chromosoma Res 23:545–560

  • Charlesworth B, Charlesworth D (2000) The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci 355:1563–1572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z-PC, Jiang X-L, Wang Y-X (1995) Karyotype and banding patterns of Fea’s tree rat (Chiromyscus chiropus). Caryologia 48:9–16

    Article  Google Scholar 

  • Chen S, Zhang G, Shao C, Huang Q, Liu G, Zhang P, Song W, An N, Chalopin D, Volff JN, Hong Y, Li Q, Sha Z, Zhou H, Xie M, Yu Q, Liu Y, Xiang H, Wang N, Wu K, Yang C, Zhou Q, Liao X, Yang L, Hu Q, Zhang J, Meng L, Jin L, Tian Y, Lian J, Yang J, Miao G, Liu S, Liang Z, Yan F, Li Y, Sun B, Zhang H, Zhang J, Zhu Y, Du M, Zhao Y, Schartl M, Tang Q, Wang J (2014) Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet 46:253–260

    Article  CAS  PubMed  Google Scholar 

  • Christidis L (1986a) Chromosomal evolution within the family Estrildidae (Aves). 1. The Poephilae. Genetica 71:81–97

    Article  Google Scholar 

  • Christidis L (1986b) Chromosomal evolution within the family Estrildidae (Aves). 2. The Lonchurae. Genetica 71:99–113

    Article  Google Scholar 

  • Cioffi MB, Bertollo LAC (2010) Initial steps in XY chromosome differentiation in Hoplias malabaricus and the origin of an X1X2Y sex chromosome system in this fish group. Heredity 105:554–561

    Article  CAS  PubMed  Google Scholar 

  • Cioffi MB, Camacho JP, Bertollo LA (2011) Repetitive DNAs and differentiation of sex chromosomes in Neotropical fishes. Cytogenet Genome Res 132:188–194

    Article  CAS  PubMed  Google Scholar 

  • Cioffi MB, Moreira-Filho O, Almeida-Toledo LF, Bertollo LA (2012) The contrasting role of heterochromatin in the differentiation of sex chromosomes: an overview from Neotropical fishes. J Fish Biol 80:2125–2139

    Article  CAS  PubMed  Google Scholar 

  • Cole CJ, Lowe CH, Wright JW (1967) Sex chromosomes in lizards. Science 155:1028–1029

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • da Rosa R, Bellafronte E, Moreira Filho O, Margarido VP (2006) Constitutive heterochromatin, 5S and 18S rDNA genes in Apareiodon sp. (Characiformes, Parodontidae) with a ZZ/ZW sex chromosome system. Genetica 128:159–166

    Article  PubMed  CAS  Google Scholar 

  • Dantas SMMdM, Barros RMdS (1997) Cytogenetic study of the genus Saguinus (Callithrichidae, Primates). Braz J Genet. doi:10.1590/S0100-84551997000400014

  • Davidson WS, Huang TK, Fujiki K, von Schalburg KR, Koop BF (2009) The sex determining loci and sex chromosomes in the family Salmonidae. Sex Dev 3:78–87

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Almeida Toledo LF, Foresti F (2001) Morphologically differentiated sex chromosomes in Neotropical freshwater fish. Genetica 111:91–100

    Article  PubMed  Google Scholar 

  • Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364

    Article  CAS  Google Scholar 

  • Elder JFJ, Turner BJ, Thomerson JE, Taphorn DC (1991) Chromosomal divergence and heterogameity in two annual killifishes of the genus Pterolebias. Genome 34:674–676

    Article  Google Scholar 

  • Ellegren H (2011) Sex-chromosome evolution: recent progress and the influence of male and female heterogamety. Nat Rev Genet 12:157–166

    Article  CAS  PubMed  Google Scholar 

  • Ezaz T, Stiglec R, Veyrunes F, Marshall Graves JA (2006) Relationships between vertebrate ZW and XY sex chromosome systems. Curr Biol 16:R736–743

    Article  CAS  PubMed  Google Scholar 

  • Ezaz T, Sarre SD, O’Meally D, Graves JA, Georges A (2009) Sex chromosome evolution in lizards: independent origins and rapid transitions. Cytogenet Genome Res 127:249–260

    Article  CAS  PubMed  Google Scholar 

  • Faber-Hammond JJ, Phillips RB, Brown KH (2015) Comparative analysis of the shared sex-determination region (SDR) among salmonid fishes. Genome Biol Evol 7:1972–1987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fredga K (1970) Unusual sex chromosome inheritance in mammals. Philos Trans R Soc Lond B Biol Sci 259:15–36

    Article  CAS  PubMed  Google Scholar 

  • Gamble T (2010) A review of sex determining mechanisms in geckos (Gekkota: Squamata). Sex Dev 4:88–103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilbert C, Goodman SM, Soarimalala V, Olson LE, O’Brien PC, Elder FF, Yang F, Ferguson-Smith MA, Robinson TJ (2007) Chromosomal evolution in tenrecs (Microgale and Oryzorictes, Tenrecidae) from the Central Highlands of Madagascar. Chromosome Res 15:1075–1091

    Article  CAS  PubMed  Google Scholar 

  • Goldoni D, Rubini M, Fontana F (1984) Cytogenetic studies on Cervus elaphus L. Constitutive heterochromatin and nucleolus organizer regions. Caryologia 37:439–443

    Article  Google Scholar 

  • Gornung E, Volleth M, Capanna E, Castiglia R (2008) Comparative cytogenetics of moles (Eulipotyphla, Talpidae): chromosomal differences in Talpa romana and T. europaea. Cytogenet Genome Res 121:249–254

    Article  CAS  PubMed  Google Scholar 

  • Graphodatsky A (1989) Appendix1. An atlas of selected karyotypes; section 1. In: Halnan CRE (ed) Cytogenetics of animals. C.A.B. International., pp 321–352

    Google Scholar 

  • Graves JA (2006) Sex chromosome specialization and degeneration in mammals. Cell 124:901–914

    Article  PubMed  CAS  Google Scholar 

  • Gray BA, Zori RT, McGuire PM, Bonde RK (2002) A first generation cytogenetic ideogram for the Florida manatee (Trichechus manatus latirostris) based on multiple chromosome banding techniques. Hereditas 137:215–223

    Article  Google Scholar 

  • Green DM (2002) Chromosome polymorphism in archey’s frog (Leiopelma archeyi) from New Zealand. Copeia 2002:204–207

  • Gutierrez JB, Teem JL (2006) A model describing the effect of sex-reversed YY fish in an established wild population: the use of a Trojan Y chromosome to cause extinction of an introduced exotic species. J Theor Biol 241:333–341

    Article  CAS  PubMed  Google Scholar 

  • Hillis DM, Green DM (1990) Evolutionary changes of heterogametic sex in the phylogenetic history of amphibians. J Evol Biol 3:49–64

    Article  Google Scholar 

  • Honda T, Suzuk iH, Itoh M (1977) An unusual sex chromosome constitution found in the Amami spinous country-rat, Tokudaia osimensis osimensis. Jap J Genet 52:247–249

    Article  Google Scholar 

  • Houck ML, Kingswood SC, Kumamoto AT (2000) Comparative cytogenetics of tapirs, genus Tapirus (Perissodactyla, Tapiridae). Cytogenet Cell Genet 89:110–115

    Article  CAS  PubMed  Google Scholar 

  • Houck ML, Kumamoto AT, Gallagher DS Jr, Benirschke K (2001) Comparative cytogenetics of the African elephant (Loxodonta africana) and Asiatic elephant (Elephas maximus). Cytogenet Cell Genet 93:249–252

    Article  CAS  PubMed  Google Scholar 

  • Hough J, Hollister JD, Wang W, Barrett SC, Wright SI (2014) Genetic degeneration of old and young Y chromosomes in the flowering plant Rumex hastatulus. Proc Natl Acad Sci U S A 111:7713–7718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang CR, Burns KH, Boeke JD (2012) Active transposition in genomes. Annu Rev Genet 46:651–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes JF, Rozen S (2012) Genomics and genetics of human and primate y chromosomes. Annu Rev Genomics Hum Genet 13:83–108

    Article  CAS  PubMed  Google Scholar 

  • Hughes JF, Skaletsky H, Pyntikova T, Graves TA, van Daalen SK, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones KW, Singh L (1985) Snakes and the evolution of sex-chromosomes. Trends Genet 1:55–61

    Article  Google Scholar 

  • Just W, Baumstark A, Suss A, Graphodatsky A, Rens W, Schafer N, Bakloushinskaya I, Hameister H, Vogel W (2007) Ellobius lutescens: sex determination and sex chromosome. Sex Dev 1:211–221

    Article  CAS  PubMed  Google Scholar 

  • Kallman K (1984) A new look at sex determination in poeciliid fishes. In: Turner B (ed) Evolutionary genetics of fishes. Plenum, New York, pp 95–171

    Chapter  Google Scholar 

  • Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, Mizuno N, Fujita M, Suetake H, Suzuki S, Hosoya S, Tohari S, Brenner S, Miyadai T, Venkatesh B, Suzuki Y, Kikuchi K (2012) A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet 8:e1002798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawagoshi T, Nishida C, Matsuda Y (2012) The origin and differentiation process of X and Y chromosomes of the black marsh turtle (Siebenrockiella crassicollis, Geoemydidae, Testudines). Chromosome Res 20:95–110

    Article  CAS  PubMed  Google Scholar 

  • Kawagoshi T, Uno Y, Nishida C, Matsuda Y (2014) The Staurotypus turtles and Aves share the same origin of sex chromosomes but evolved different types of heterogametic sex determination. PLoS One 9:e105315

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kawai A, Nishida-Umehara C, Ishijima J, Tsuda Y, Ota H, Matsuda Y (2007) Different origins of bird and reptile sex chromosomes inferred from comparative mapping of chicken Z-linked genes. Cytogenet Genome Res 117:92–102

    Article  CAS  PubMed  Google Scholar 

  • Kejnovský E, Michalovova M, Steflova P, Kejnovska I, Manzano S, Hobza R, Kubat Z, Kovarik J, Jamilena M, Vyskot B (2013) Expansion of microsatellites on evolutionary young Y chromosome. PLoS One 8:e45519

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • King M (1977) The evolution of sex chromosomes in lizards. In: Calaly J, Tyndale-Biscoe H (eds) Evolution and reproduction. Australian Academy of Science, Canberra, pp 55–60

    Google Scholar 

  • King M (1990) Chromosomal and immunogenetic data: a new perspective on the origin of Australia’s reptiles. In: Olmo E (ed) Cytogenetics of amphibians and reptiles. Birkhäuser, Basel, pp 153–180

    Google Scholar 

  • Kobayashi Y, Nagahama Y, Nakamura M (2013) Diversity and plasticity of sex determination and differentiation in fishes. Sex Dev 7:115–125

    Article  CAS  PubMed  Google Scholar 

  • Koehler MR, Dehm D, Guttenbach M, Nanda I, Haaf T, Molina WF, Galetti PM Jr, Schmid M (1997) Cytogenetics of the genus Leporinus (Pisces, Anostomidae). 1. Karyotype analysis, heterochromatin distribution and sex chromosomes. Chromosome Res 5:12–22

    Article  CAS  PubMed  Google Scholar 

  • Kondo M, Nagao E, Mitani H, Shima A (2001) Differences in recombination frequencies during female and male meioses of the sex chromosomes of the medaka, Oryzias latipes. Genet Res 78:23–30

    Article  CAS  PubMed  Google Scholar 

  • Kondo M, Nanda I, Hornung U, Schmid M, Schartl M (2004) Evolutionary origin of the medaka Y chromosome. Curr Biol 14:1664–1669

    Article  CAS  PubMed  Google Scholar 

  • Kondo M, Hornung U, Nanda I, Imai S, Sasaki T, Shimizu A, Asakawa S, Hori H, Schmid M, Shimizu N, Schartl M (2006) Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka. Genome Res 16:815–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Konerat J, Bueno V, Margarido V, de Brito Portela-Castro A, Martins-Santos I (2015) Diversity sex chromosome systems in Ancistrini (Loricariidae, Hypostominae): ZZ/ZW in Ancistrus taunayi Miranda Ribeiro, 1918. Cytogen Genome Res: in press.

  • Lahn BT, Page DC (1999) Four evolutionary strata on the human X chromosome. Science 286:964–967

    Article  CAS  PubMed  Google Scholar 

  • Liu JD, Yi MS, Zhao G, Zhou F, Wang DQ, Yu QX (2002) Sex chromosomes in the spiny eel (Mastacembelus aculeatus) revealed by mitotic and meiotic analysis. Cytogenet Genome Res 98:291–297

    Article  CAS  PubMed  Google Scholar 

  • Livernois AM, Graves JA, Waters PD (2012) The origin and evolution of vertebrate sex chromosomes and dosage compensation. Heredity 108:50–58

    Article  CAS  PubMed  Google Scholar 

  • Lubieniecki KP, Lin S, Cabana EI, Li J, Lai YY, Davidson WS (2015) Genomic instability of the sex-determining locus in Atlantic salmon (Salmo salar). G3 (Bethesda) 5:2513–2522

    Article  Google Scholar 

  • Mahony MJ (1991) Heteromorphic sex-chromosomes in the Australian frog Crinia bilingua (Anura, Myobatrachidae). Genome 34:334–337

    Article  Google Scholar 

  • Mank JE, Avise JC (2009) Evolutionary diversity and turn-over of sex determination in teleost fishes. Sex Dev 3:60–67

    Article  CAS  PubMed  Google Scholar 

  • Marshall Graves JA, Shetty S (2001) Sex from W to Z: evolution of vertebrate sex chromosomes and sex determining genes. J Exp Zool 290:449–462

    Article  CAS  PubMed  Google Scholar 

  • Matsubara K, Tarui H, Toriba M, Yamada K, Nishida-Umehara C, Agata K, Matsuda Y (2006) Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes. Proc Natl Acad Sci U S A 103:18190–18195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsubara K, Knopp T, Sarre SD, Georges A, Ezaz T (2013) Karyotypic analysis and FISH mapping of microsatellite motifs reveal highly differentiated XX/XY sex chromosomes in the pink-tailed worm-lizard (Aprasia parapulchella, Pygopodidae, Squamata). Mol Cytogenet 6:60

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Matsubara K, Sarre SD, Georges A, Matsuda Y, Marshall Graves JA, Ezaz T (2014) Highly differentiated ZW sex microchromosomes in the Australian Varanus species evolved through rapid amplification of repetitive sequences. PLoS One 9:e95226

    Article  PubMed  PubMed Central  Google Scholar 

  • Matsubara K, O’Meally D, Azad B, Georges A, Sarre SD, Graves JA, Matsuda Y, Ezaz T (2015) Amplification of microsatellite repeat motifs is associated with the evolutionary differentiation and heterochromatinization of sex chromosomes in Sauropsida. Chromosoma: [Epub ahead of print]

  • Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417:559–563

    Article  CAS  PubMed  Google Scholar 

  • Matthey R (1953) La formule chromosomique et le problème de la détermination sexuelle chez Ellobius lutescens Thomas (Rodentia-Muridae-Microtinae). Arch Klaus-Stift Vererb-Forsch 28:65–73

    Google Scholar 

  • Mengden GA, Stock AD (1980) Chromosomal evolution in Serpentes—a comparison of chromosome-G and chromosome-C banding-patterns of some colubrid and boid genera. Chromosoma 79:53–64

    Article  Google Scholar 

  • Mohanty MK, Bhunya SP (1990) Karyological studies in 4 species of Ardeid birds (Ardeidae, Ciconiiformes). Genetica 81:211–214

    Article  Google Scholar 

  • Moritz C (1984) The evolution of a highly variable sex chromosome in Gehyra purpurascens (Gekkonidae). Chromosoma 90:111–119

    Article  Google Scholar 

  • Murata C, Yamada F, Kawauchi N, Matsuda Y, Kuroiwa A (2012) The Y chromosome of the Okinawa spiny rat, Tokudaia muenninki, was rescued through fusion with an autosome. Chromosome Res 20:111–125

    Article  CAS  PubMed  Google Scholar 

  • Nagamachi CY, Pieczarka JC (1988) Chromosome studies of Saguinus midas niger (Callithricidae, Primates) from Tucurui, Para, Brazil: comparison with the karyotype of Callithrix jacchus. Am J Primatology 14:277–284

    Article  Google Scholar 

  • Nanda I, Feichtinger W, Schmid M, Schröder JH, Zischler H, Epplen JT (1990) Simple repetitive sequences are associated with differentiation of the sex-chromosomes in the guppy fish. J Mol Evol 30:456–462

    Article  CAS  Google Scholar 

  • Nanda I, Shan Z, Schartl M, Burt DW, Koehler M, Nothwang H, Grutzner F, Paton IR, Windsor D, Dunn I, Engel W, Staeheli P, Mizuno S, Haaf T, Schmid M (1999) 300 million years of conserved synteny between chicken Z and human chromosome 9. Nat Genet 21:258–259

    Article  CAS  PubMed  Google Scholar 

  • Nanda I, Volff JN, Weis S, Körting C, Froschauer A, Schmid M, Schartl M (2000) Amplification of a long terminal repeat-like element on the Y chromosome of the platyfish, Xiphophorus maculatus. Chromosoma 109:173–180

    Article  CAS  PubMed  Google Scholar 

  • Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shan Z, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M (2002) A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci U S A 99:11778–11783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nanda I, Schlegelmilch K, Haaf T, Schartl M, Schmid M (2008) Synteny conservation of the Z chromosome in 14 avian species (11 families) supports a role for Z dosage in avian sex determination. Cytogenet Genome Res 122:150–156

    Article  CAS  PubMed  Google Scholar 

  • Nanda I, Schories S, Tripathi N, Dreyer C, Haaf T, Schmid M, Schartl M (2014) Sex chromosome polymorphism in guppies. Chromosoma 123:373–383

    Article  CAS  PubMed  Google Scholar 

  • Nascimento J, Quindere YRSD, Recco-Pimentel SM, Lima JRF, Lourenco LB (2010) Heteromorphic Z and W sex chromosomes in Physalaemus ephippifer (Steindachner, 1864) (Anura, Leiuperidae). Genetica 138:1127–1132

    Article  PubMed  Google Scholar 

  • Nieto LM, Kretschmer R, Ledesma MA, Garnero ADV, Gunsk iRJ (2012) Karyotype morphology suggests that the Nyctibius griseus (Gmelin, 1789) carries an ancestral ZW-chromosome pair to the order Caprimulgiformes (Aves). Comp Cytogenetics 6:379–387

    Article  Google Scholar 

  • Nishida-Umehara C, Tsuda Y, Ishijima J, Ando J, Fujiwara A, Matsuda Y, Griffin DK (2007) The molecular basis of chromosome orthologies and sex chromosomal differentiation in palaeognathous birds. Chromosome Res 15:721–734

    Article  CAS  PubMed  Google Scholar 

  • Noleto RB, Amorim AP, Vicari MR, Artoni RF, Cestari MM (2009) An unusual ZZ/ZW sex chromosome system in Characidium fishes (Crenuchidae, Characiformes) with the presence of rDNA sites. J Fish Biol 75:448–453

    Article  CAS  PubMed  Google Scholar 

  • Ohno S (1967) Sex chromosomes and sex-linked genes. Springer, Berlin

    Book  Google Scholar 

  • Oliveira C, Toledo LFD (2006) Evidence of an XX/XY sex chromosome system in the fish Dormitator maculatus (Teleostei, Eleotrididae). Genet Mol Biol 29:653–655

    Article  Google Scholar 

  • Oliveira RR, Feldberg E, Anjos MB, Zuanon J (2007) Karyotype characterization and ZZ/ZW sex chromosome heteromorphism in two species of the catfish genus Ancistrus Kner, 1854 (Siluriformes: Loricariidae) from the Amazon basin. Neotrop Ichthyol 5:301–306

    Article  Google Scholar 

  • Olmo E, Odierna G, Capriglione T (1987) Evolution of sex-chromosomes in lacertid lizards. Chromosoma 96:33–38

    Article  Google Scholar 

  • O’Meally D, Patel HR, Stiglec R, Sarre SD, Georges A, Marshall Graves JA, Ezaz T (2010) Non-homologous sex chromosomes of birds and snakes share repetitive sequences. Chromosome Res 18:787–800

    Article  PubMed  CAS  Google Scholar 

  • Pala I, Naurin S, Stervander M, Hasselquist D, Bensch S, Hansson B (2012) Evidence of a neo-sex chromosome in birds. Heredity 108:264–272

    Article  CAS  PubMed  Google Scholar 

  • Parise-Maltempi PP, da Silva EL, Rens W, Dearden F, O’Brien PC, Trifonov V, Ferguson-Smith MA (2013) Comparative analysis of sex chromosomes in Leporinus species (Teleostei, Characiformes) using chromosome painting. BMC Genet 14:60

    Article  PubMed  PubMed Central  Google Scholar 

  • Peichel CL, Ross JA, Matson CK, Dickson M, Grimwood J, Schmutz J, Myers RM, Mori S, Schluter D, Kingsley DM (2004) The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Curr Biol 14:1416–1424

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Phillips RB (2013) Evolution of the sex chromosomes in salmonid fishes. Cytogenet Genome Res 141:177–185

    Article  CAS  PubMed  Google Scholar 

  • Pokorná M, Kratochvíl L, Kejnovský E (2011) Microsatellite distribution on sex chromosomes at different stages of heteromorphism and heterochromatinization in two lizard species (Squamata: Eublepharidae: Coleonyx elegans and Lacertidae: Eremias velox). BMC Genet 12:90

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pokorná M, Rens W, Rovatsos M, Kratochvíl L (2014) A ZZ/ZW sex chromosome system in the thick-tailed Gecko (Underwoodisaurus milii; Squamata: Gekkota: Carphodactylidae), a member of the ancient gecko lineage. Cytogenet Genome Res 142:190–196

    PubMed  Google Scholar 

  • Raman R, Nanda I (1982) Identification and patterns of synapsis of the autosomally translocated Y-chromosome of the Indian mongoose, Herpestes auropunctatus (Hodgson). Chromosoma 87:477–489

    Article  CAS  PubMed  Google Scholar 

  • Raman R, Nanda I (1986) Mammalian sex chromosomes. I. Cytological changes in the chiasmatic sex chromosomes of the male musk shrew, Suncus murinus. Chromosoma 93:367–374

    Article  CAS  PubMed  Google Scholar 

  • Rice WR (1996) Evolution of the Y sex chromosome in animals. BioScience 46:331–343

    Article  Google Scholar 

  • Roco AS, Olmstead AW, Degitz SJ, Amano T, Zimmerman LB, Bullejos M (2015) Coexistence of Y, W, and Z sex chromosomes in Xenopus tropicalis. Proc Natl Acad Sci U S A 112:E4752–4761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ross JA, Urton JR, Boland J, Shapiro MD, Peichel CL (2009) Turnover of sex chromosomes in the stickleback fishes (Gasterosteidae). Plos Genetics 5:e1000391

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rossi LF, Luaces JP, Alonso FM, Merani MS (2014) Karyotype and chromosome variability in the armadillo Chaetophractus villosus in Argentina. Cytogenet Genome Res 142:101–106

    Article  CAS  PubMed  Google Scholar 

  • Rovatsos M, Pokorna M, Altmanova M, Kratochvil L (2014) Cretaceous park of sex determination: sex chromosomes are conserved across iguanas. Biol Lett 10:20131093

    Article  PubMed  PubMed Central  Google Scholar 

  • Rovatsos M, Johnson Pokorna M, Altmanova M, Kratochvil L (2015) Female heterogamety in Madagascar chameleons (Squamata: Chamaeleonidae: Furcifer): differentiation of sex and neo-sex chromosomes. Sci Rep 5:13196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rutkowska J, Lagisz M, Nakagawa S (2012) The long and the short of avian W chromosomes: no evidence for gradual W shortening. Biol Lett 8:636–638

    Article  PubMed  PubMed Central  Google Scholar 

  • Sato T, Endo T, Yamahira K, Hamaguchi S, Sakaizumi M (2005) Induction of female-to-male sex reversal by high temperature treatment in Medaka, Oryzias latipes. Zoolog Sci 22:985–988

    Article  PubMed  Google Scholar 

  • Schempp W, Schmid M (1981) Chromosome-banding in Amphibia. 6. Brdu-replication patterns in Anura and demonstration of Xx-Xy Sex-chromosomes in Rana esculenta. Chromosoma 83:697–710

    Article  CAS  PubMed  Google Scholar 

  • Schmid M (1980) Chromosome-banding in Amphibia. V. Highly differentiated ZW/ZZ sex chromosomes and exceptional genome size in Pyxicephalus adspersus (Anura, Ranidae). Chromosoma 80:69–96

    Article  CAS  Google Scholar 

  • Schmid M, Olert J, Klett C (1979) Chromosome banding in Amphibia. III sex chromosomes in Triturus. Chromosoma 71:29–55

    Article  Google Scholar 

  • Schmid M, Haaf T, Geile B, Sims S (1983) Chromosome banding in Amphibia. VIII. An unusual XY/XX-sex chromosome system in Gastrotheca riobambae (Anura, Hylidae). Chromosoma 88:69–82

    Article  CAS  PubMed  Google Scholar 

  • Schmid M, Ohta S, Steinlein C, Guttenbach M (1993) Chromosome banding in Amphibia. XIX. Primitive ZW/ZZ sex chromosomes in Buergeria buergeri (Anura, Rhacophoridae). Cytogenet Cell Genet 62:238–246

    Article  CAS  PubMed  Google Scholar 

  • Schmid M, Feichtinger W, Steinlein C, Nanda I, Mais C, Haaf T, Visbal Garcia R, Fernandez Badillo A (2002a) Chromosome banding in Amphibia. XXII. Atypical y chromosomes in Gastrotheca walkeri and Gastrotheca ovifera (Anura, Hylidae). Cytogenet Genome Res 96:228–238

    Article  CAS  PubMed  Google Scholar 

  • Schmid M, Feichtinger W, Steinlein C, Rupprecht A, Haaf T, Kaiser H (2002b) Chromosome banding in Amphibia. XXIII. Giant W sex chromosomes and extremely small genomes in Eleutherodactylus euphronides and Eleutherodactylus shrevei (Anura, Leptodactylidae). Cytogenet Genome Res 97:81–94

    Article  CAS  PubMed  Google Scholar 

  • Schmid M, Steinlein C, Bogart JP, Feichtinger W, Leon P, La Marca E, Diaz LM, Sanz A, Chen SH, Hedges SB (2010) The chromosomes of terraranan frogs. Insights into vertebrate cytogenetics. Cytogenet Genome Res 130–131:1–568

    Article  PubMed  Google Scholar 

  • Schmid M, Steinlein C, Haaf T, Mijares-Urrutia A (2014) Nascent ZW sex chromosomes in Thecadactylus rapicauda (Reptilia, Squamata, Phyllodactylidae). Cytogenet Genome Res 143:259–267

    PubMed  Google Scholar 

  • Sessions SK (1980) Evidence for a highly differentiated sex-chromosome heteromorphism in the salamander Necturus maculosus (Rafinesque). Chromosoma 77:157–168

    Article  Google Scholar 

  • Shinomiya A, Otake H, Hamaguchi S, Sakaizumi M (2010) Inherited XX sex reversal originating from wild medaka populations. Heredity 105:443–448

    Article  CAS  PubMed  Google Scholar 

  • Singh L (1972) Evolution of karyotypes in snakes. Chromosoma 38:185

    Article  CAS  PubMed  Google Scholar 

  • Singh L, Purdom IF, Jones KW (1976) Satellite DNA and evolution of sex chromosomes. Chromosoma 59:43–62

    Article  CAS  PubMed  Google Scholar 

  • Singh L, Purdom IF, Jones KW (1980) Sex-chromosome associated satellite DNA—evolution and conservation. Chromosoma 79:137–157

    Article  CAS  PubMed  Google Scholar 

  • Soh YQ, 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 159:800–813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solano E, Taylor PJ, Rautenbach A, Ropiquet A, Castiglia R (2014) Cryptic speciation and chromosomal repatterning in the South African climbing mice Dendromus (Rodentia, Nesomyidae). PLoS One 9:e88799

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Splendore de Borba R, Lourenco da Silva E, Parise-Maltempi PP (2013) Chromosome mapping of retrotransposable elements and in Spix, 1829 species (Characiformes: Anostomidae) and its relationships among heterochromatic segments and W sex chromosome. Mob Genet Elements 3:e27460

    Article  PubMed  PubMed Central  Google Scholar 

  • Srikulnath K, Nishida C, Matsubara K, Uno Y, Thongpan A, Suputtitada S, Apisitwanich S, Matsuda Y (2009) Karyotypic evolution in squamate reptiles: comparative gene mapping revealed highly conserved linkage homology between the butterfly lizard (Leiolepis reevesii rubritaeniata, Agamidae, Lacertilia) and the Japanese four-striped rat snake (Elaphe quadrivirgata, Colubridae, Serpentes). Chromosome Res 17:975–986

    Article  CAS  PubMed  Google Scholar 

  • Stöck M, Horn A, Grossen C, Lindtke D, Sermier R, Betto-Colliard C, Dufresnes C, Bonjour E, Dumas Z, Luquet E, Maddalena T, Sousa HC, Martinez-Solano I, Perrin N (2011) Ever-young sex chromosomes in European tree frogs. PLoS Biol 9:e1001062

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Suarez-Villota EY, Pansonato-Alves JC, Foresti F, Gallardo MH (2014) Homomorphic sex chromosomes and the intriguing Y chromosome of Ctenomys rodent species (Rodentia, Ctenomyidae). Cytogenet Genome Res 143:232–240

    PubMed  Google Scholar 

  • Swarca AC, Fenocchio AS, Cestari MM, Bertollo LAC, Dias AL (2006) Heteromorphic sex chromosome system with an exceptionally large Y chromosome in a catfish Steindachneridion sp (Pimelodidae). Cytogenet Genome Res 112:325–328

    Article  CAS  PubMed  Google Scholar 

  • Takeda H (2008) Draft genome of the medaka fish: a comprehensive resource for medaka developmental genetics and vertebrate evolutionary biology. Dev Growth Differ 50(Suppl 1):S157–166

    Article  CAS  PubMed  Google Scholar 

  • Takehana Y, Naruse K, Hamaguchi S, Sakaizumi M (2007) Evolution of ZZ/ZW and XX/XY sex-determination systems in the closely related medaka species, Oryzias hubbsi and O. dancena. Chromosoma 116:463–470

    Article  PubMed  Google Scholar 

  • Terencio ML, Schneider CH, Gross MC, Nogaroto V, de Almeida MC, Artoni RF, Vicari MR, Feldberg E (2012) Repetitive sequences associated with differentiation of W chromosome in Semaprochilodus taeniurus. Genetica 140:505–512

    Article  CAS  PubMed  Google Scholar 

  • Terencio ML, Schneider CH, Gross MC, Vicari MR, Farias IP, Passos KB, Feldberg E (2013) Evolutionary dynamics of repetitive DNA in Semaprochilodus (Characiformes, Prochilodontidae): a fish model for sex chromosome differentiation. Sex Dev 7:325–333

    Article  CAS  PubMed  Google Scholar 

  • Tsuda Y, Nishida-Umehara C, Ishijima J, Yamada K, Matsuda Y (2007) Comparison of the Z and W sex chromosomal architectures in elegant crested tinamou (Eudromia elegans) and ostrich (Struthio camelus) and the process of sex chromosome differentiation in palaeognathous birds. Chromosoma 116:159–173

    Article  PubMed  Google Scholar 

  • Uno Y, Nishida C, Oshima Y, Yokoyama S, Miura I, Matsuda Y, Nakamura M (2008) Comparative chromosome mapping of sex-linked genes and identification of sex chromosomal rearrangements in the Japanese wrinkled frog (Rana rugosa, Ranidae) with ZW and XY sex chromosome systems. Chromosome Res 16:637–647

    Article  CAS  PubMed  Google Scholar 

  • Venere PC, Souza IL, Martins C, Oliveira C (2008) Occurrence of ZZ/ZW sex chromosomes in Thoracocharax stellatus fish (Characiformes, Gasteropelecidae) from the Araguaia River, South America. Genetica 133:109–112

    Article  PubMed  Google Scholar 

  • Vicente VE, Bertollo LA, Valentini SR, Filho OM (2003) Origin and differentiation of a sex chromosome system in Parodon hilarii (Pisces, Parodontidae). Satellite DNA, G- and C-banding. Genetica 119:115–120

    Article  CAS  PubMed  Google Scholar 

  • Vicoso B, Emerson JJ, Zektser Y, Mahajan S, Bachtrog D (2013) Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol 11:e1001643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vistorin G, Gamperl R, Rosenkranz W (1977) Studies on sex chromosomes of four hamster species: Cricetus cricetus, Cricetulus griseus, Mesocricetus auratus, and Phodopus sungorus. Cytogenet Cell Genet 18:24–32

    Article  CAS  PubMed  Google Scholar 

  • Volff JN, Körting C, Froschauer A, Zhou Q, Wilde B, Schultheis C, Selz Y, Sweeney K, Duschl J, Wichert K, Altschmied J, Schartl M (2003) The Xmrk oncogene can escape nonfunctionalization in a highly unstable subtelomeric region of the genome of the fish Xiphophorus. Genomics 82:470–479

    Article  CAS  PubMed  Google Scholar 

  • Volff JN, Nanda I, Schmid M, Schartl M (2007) Governing sex determination in fish: regulatory putsches and ephemeral dictators. Sex Dev 1:85–99

    Article  PubMed  Google Scholar 

  • Wilson CA, High SK, McCluskey BM, Amores A, Yan YL, Titus TA, Anderson JL, Batzel P, Carvan MJ 3rd, Schartl M, Postlethwait JH (2014) Wild sex in zebrafish: loss of the natural sex determinant in domesticated strains. Genetics 198:1291–1308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woram RA, Gharbi K, Sakamoto T, Hoyheim B, Holm LE, Naish K, McGowan C, Ferguson MM, Phillips RB, Stein J, Guyomard R, Cairney M, Taggart JB, Powell R, Davidson W, Danzmann RG (2003) Comparative genome analysis of the primary sex-determining locus in salmonid fishes. Genome Res 13:272–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiu-Guang M, Jin-Huan W, Wei-Ting S, Ying-Xiang W, Feng-Tang Y, Wen-Hui N (2010) Karyotypic evolution in family Hipposideridae (Chiroptera, Mammalia) revealed by comparative chromosome painting, G- and C-banding. Zool Res 31:453–460

    Google Scholar 

  • Yamada K, Nishida-Umehara C, Matsuda Y (2004) A new family of satellite DNA sequences as a major component of centromeric heterochromatin in owls (Strigiformes). Chromosoma 112:277–287

    Article  CAS  PubMed  Google Scholar 

  • Yano A, Guyomard R, Nicol B, Jouanno E, Quillet E, Klopp C, Cabau C, Bouchez O, Fostier A, Guiguen Y (2012) An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr Biol 22:1423–1428

    Article  CAS  PubMed  Google Scholar 

  • Yano A, Nicol B, Jouanno E, Quillet E, Fostier A, Guyomard R, Guiguen Y (2013) The sexually dimorphic on the Y-chromosome gene (sdY) is a conserved male-specific Y-chromosome sequence in many salmonids. Evol Appl 6:486–496

    Article  CAS  PubMed  Google Scholar 

  • Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, Nishida-Umehara C, Matsuda Y, Takamatsu N, Shiba T, Ito M (2008) A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci U S A 105:2469–2474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Q, Braasch I, Froschauer A, Bohne A, Schultheis C, Schartl M, Volff JN (2010) A novel marker for the platyfish (Xiphophorus maculatus) W chromosome is derived from a Polinton transposon. J Genet Genomics 37:181–188

    Article  CAS  PubMed  Google Scholar 

  • Zhou Q, Zhang J, Bachtrog D, An N, Huang Q, Jarvis ED, Gilbert MT, Zhang G (2014) Complex evolutionary trajectories of sex chromosomes across bird taxa. Science 346:1246338

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Information collected on sex chromosomes of many weird species through numerous cytogenetic colleagues from many countries is highly appreciated. The list of examples for sex chromosomes discussed in this review that deviate from the classical view is certainly not complete. We apologize to all our colleagues whose work have escaped our attention and have not been mentioned appropriately. We thank Monika Niklaus-Ruiz for the help in the preparation of the manuscript. The work of the authors on sex chromosomes has been supported by the DFG through grants SCHA 408/12-1 and SCHA 408/10-1.

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  1. Physiological Chemistry, University of Würzburg, Biocenter, Am Hubland, Würzburg, Germany

    Manfred Schartl

  2. Comprehensive Cancer Center Mainfranken, University Clinic, Würzburg, Germany

    Manfred Schartl

  3. Institute for Human Genetics, University of Würzburg, Biocenter, Am Hubland, Würzburg, Germany

    Michael Schmid & Indrajit Nanda

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  1. Manfred Schartl
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Correspondence to Manfred Schartl.

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Schartl, M., Schmid, M. & Nanda, I. Dynamics of vertebrate sex chromosome evolution: from equal size to giants and dwarfs. Chromosoma 125, 553–571 (2016). https://doi.org/10.1007/s00412-015-0569-y

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