Deciphering the Origin and Evolution of the X1X2Y System in Two Closely-Related Oplegnathus Species (Oplegnathidae and Centrarchiformes)

Oplegnathus fasciatus and O. punctatus (Teleostei: Centrarchiformes: Oplegnathidae), are commercially important rocky reef fishes, endemic to East Asia. Both species present an X1X2Y sex chromosome system. Here, we investigated the evolutionary forces behind the origin and differentiation of these sex chromosomes, with the aim to elucidate whether they had a single or convergent origin. To achieve this, conventional and molecular cytogenetic protocols, involving the mapping of repetitive DNA markers, comparative genomic hybridization (CGH), and whole chromosome painting (WCP) were applied. Both species presented similar 2n, karyotype structure and hybridization patterns of repetitive DNA classes. 5S rDNA loci, besides being placed on the autosomal pair 22, resided in the terminal region of the long arms of both X1 chromosomes in females, and on the X1 and Y chromosomes in males. Furthermore, WCP experiments with a probe derived from the Y chromosome of O. fasciatus (OFAS-Y) entirely painted the X1 and X2 chromosomes in females and the X1, X2, and Y chromosomes in males of both species. CGH failed to reveal any sign of sequence differentiation on the Y chromosome in both species, thereby suggesting the shared early stage of neo-Y chromosome differentiation. Altogether, the present findings confirmed the origin of the X1X2Y sex chromosomes via Y-autosome centric fusion and strongly suggested their common origin.

[1]  T. Liehr,et al.  Comparative Cytogenetics and Neo-Y Formation in Small-Sized Fish Species of the Genus Pyrrhulina (Characiformes, Lebiasinidae) , 2019, Front. Genet..

[2]  M. Cioffi,et al.  Evolution of Bird Sex Chromosomes Narrated by Repetitive Sequences: Unusual W Chromosome Enlargement in Gallinula melanops (Aves: Gruiformes: Rallidae) , 2019, Cytogenetic and Genome Research.

[3]  M. Ferguson-Smith,et al.  Identification of two independent X-autosome translocations in closely related mammalian (Proechimys) species , 2019, Scientific Reports.

[4]  R. Elias,et al.  High Dialysate Calcium Concentration is Associated with Worsening Left Ventricular Function , 2019, Scientific Reports.

[5]  J. Postlethwait,et al.  Identification of the master sex determining gene in Northern pike (Esox lucius) reveals restricted sex chromosome differentiation , 2019, bioRxiv.

[6]  Jun Li,et al.  Genome sequence of the barred knifejaw Oplegnathus fasciatus (Temminck & Schlegel, 1844): the first chromosome-level draft genome in the family Oplegnathidae , 2019, GigaScience.

[7]  S. Lien,et al.  Characterization of a male specific region containing a candidate sex determining gene in Atlantic cod , 2019, Scientific Reports.

[8]  S. Voss,et al.  Miniscule differences between sex chromosomes in the giant genome of a salamander , 2018, Scientific Reports.

[9]  Ho-jin Jung,et al.  First draft genome sequence of the rock bream in the family Oplegnathidae , 2018, Scientific Data.

[10]  T. Kocher,et al.  Unusual Diversity of Sex Chromosomes in African Cichlid Fishes , 2018, Genes.

[11]  T. Demidova,et al.  Extensive karyotype variability of African fish genus Nothobranchius (Cyprinodontiformes) , 2018, Comparative cytogenetics.

[12]  M. Dalíková,et al.  Sex Chromosomes of the Iconic Moth Abraxas grossulariata (Lepidoptera, Geometridae) and Its Congener A. sylvata , 2018, Genes.

[13]  Natasha I. Bloch,et al.  Shared and Species-Specific Patterns of Nascent Y Chromosome Evolution in Two Guppy Species , 2018, Genes.

[14]  C. F. Yano,et al.  Sex Chromosome Evolution and Genomic Divergence in the Fish Hoplias malabaricus (Characiformes, Erythrinidae) , 2018, Front. Genet..

[15]  V. Trifonov,et al.  Tracking the evolutionary pathway of sex chromosomes among fishes: characterizing the unique XX/XY1Y2 system in Hoplias malabaricus (Teleostei, Characiformes) , 2018, Chromosoma.

[16]  R. Symonová,et al.  Vertebrate Genome Evolution in the Light of Fish Cytogenomics and rDNAomics , 2018, Genes.

[17]  Yilei Wang,et al.  Cytogenetic characterization and description of an X1X1X2X2/X1X2Y sex chromosome system in Collichthys lucidus (Richardson, 1844) , 2018, Acta Oceanologica Sinica.

[18]  B. Fu,et al.  Sex-specific markers developed by next-generation sequencing confirmed an XX/XY sex determination system in bighead carp (Hypophthalmichthys nobilis) and silver carp (Hypophthalmichthys molitrix) , 2018, DNA research : an international journal for rapid publication of reports on genes and genomes.

[19]  T. Liehr,et al.  First Chromosomal Analysis in Hepsetidae (Actinopterygii, Characiformes): Insights into Relationship between African and Neotropical Fish Groups , 2017, Front. Genet..

[20]  G. Dias,et al.  High-throughput analysis of the satellitome revealed enormous diversity of satellite DNAs in the neo-Y chromosome of the cricket Eneoptera surinamensis , 2017, Scientific Reports.

[21]  T. Ezaz,et al.  Early Stages of XY Sex Chromosomes Differentiation in the Fish Hoplias malabaricus (Characiformes, Erythrinidae) Revealed by DNA Repeats Accumulation , 2017, Current genomics.

[22]  B. Ng,et al.  New insights into sex chromosome evolution in anole lizards (Reptilia, Dactyloidae) , 2017, Chromosoma.

[23]  A. BitencourtJamille,et al.  First Report of Sex Chromosomes in Achiridae (Teleostei: Pleuronectiformes) with Inferences About the Origin of the Multiple X1X1X2X2/X1X2Y System and Dispersal of Ribosomal Genes in Achirus achirus. , 2017 .

[24]  D. Badenhorst,et al.  Discovery of the youngest sex chromosomes reveals first case of convergent co-option of ancestral autosomes in turtles , 2017, Chromosoma.

[25]  P. Li,et al.  Karyotype analysis and ribosomal gene localization of spotted knifejaw Oplegnathus punctatus. , 2016, Genetics and molecular research : GMR.

[26]  V. Trifonov,et al.  Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae) , 2016, Heredity.

[27]  Caroline Garcia,et al.  A new multiple sex chromosome system X1X1X2X2/X1Y1X2Y2 in Siluriformes: cytogenetic characterization of Bunocephalus coracoideus (Aspredinidae) , 2016, Genetica.

[28]  R. ffrench-Constant,et al.  A neo-W chromosome in a tropical butterfly links colour pattern, male-killing, and speciation , 2016, Proceedings of the Royal Society B: Biological Sciences.

[29]  M. Rovatsos,et al.  Minute Y chromosomes and karyotype evolution in Madagascan iguanas (Squamata: Iguania: Opluridae) , 2016 .

[30]  M. Ohno,et al.  Fissions, fusions, and translocations shaped the karyotype and multiple sex chromosome constitution of the northeast-Asian wood white butterfly, Leptidea amurensis , 2016 .

[31]  M. Schartl,et al.  Dynamics of vertebrate sex chromosome evolution: from equal size to giants and dwarfs , 2016, Chromosoma.

[32]  T. Gamble.  Using RAD‐seq to recognize sex‐specific markers and sex chromosome systems , 2016, Molecular ecology.

[33]  FeldbergEliana,et al.  Cytogenetic Diversity and the Evolutionary Dynamics of rDNA Genes and Telomeric Sequences in the Ancistrus Genus (Loricariidae: Ancistrini) , 2016 .

[34]  D. Chalopin,et al.  Insights into Sex Chromosome Evolution and Aging from the Genome of a Short-Lived Fish , 2015, Cell.

[35]  R. Symonová,et al.  Karyotype differentiation in 19 species of river loach fishes (Nemacheilidae, Teleostei): extensive variability associated with rDNA and heterochromatin distribution and its phylogenetic and ecological interpretation , 2015, BMC Evolutionary Biology.

[36]  Y. Uno,et al.  No Interstitial Telomeres on Autosomes but Remarkable Amplification of Telomeric Repeats on the W Sex Chromosome in the Sand Lizard (Lacerta agilis). , 2015, The Journal of heredity.

[37]  M. Rovatsos,et al.  Interstitial Telomeric Motifs in Squamate Reptiles: When the Exceptions Outnumber the Rule , 2015, PloS one.

[38]  R. Symonová,et al.  Characterization of Fish Genomes by GISH and CGH , 2015 .

[39]  J. C. Pieczarka,et al.  X1X1X2X2/X1X2Y sex chromosome systems in the Neotropical Gymnotiformes electric fish of the genus Brachyhypopomus , 2015, Genetics and molecular biology.

[40]  D. C. Cabral-de-Mello,et al.  Repetitive DNA chromosomal organization in the cricket Cycloptiloides americanus: a case of the unusual X1X20 sex chromosome system in Orthoptera , 2015, Molecular Genetics and Genomics.

[41]  D. Diniz,et al.  A unique sex chromosome system in the knifefish Gymnotus bahianus with inferences about chromosomal evolution of Gymnotidae. , 2015, The Journal of heredity.

[42]  FeldbergEliana,et al.  New approach data in electric fish (Teleostei: Gymnotus): sex chromosome evolution and repetitive DNA. , 2014 .

[43]  Zhizhong Xiao,et al.  Pronounced population genetic differentiation in the rock bream Oplegnathus fasciatus inferred from mitochondrial DNA sequences , 2014, Mitochondrial DNA. Part A, DNA mapping, sequencing, and analysis.

[44]  M. Kirkpatrick,et al.  LOCAL ADAPTATION AND THE EVOLUTION OF CHROMOSOME FUSIONS , 2014, Evolution; international journal of organic evolution.

[45]  D. Badenhorst,et al.  Molecular Cytogenetic Search for Cryptic Sex Chromosomes in Painted Turtles Chrysemys picta , 2014, Cytogenetic and Genome Research.

[46]  T. Liehr,et al.  Genomic organization of repetitive DNAs and its implications for male karyotype and the neo-Y chromosome differentiation in Erythrinus erythrinus (Characiformes, Erythrinidae) , 2014, Comparative cytogenetics.

[47]  M. Cioffi,et al.  Chromosomal distribution of two multigene families and the unusual occurrence of an X1X1X2X2/X1X2Y sex chromosome system in the dolphinfish (Coryphaenidae): an evolutionary perspective. , 2014, Genetics and molecular research : GMR.

[48]  M. Schartl,et al.  Sex chromosome polymorphism in guppies , 2014, Chromosoma.

[49]  M. Rovatsos,et al.  A ZZ/ZW Sex Chromosome System in the Thick-Tailed Gecko (Underwoodisaurus milii; Squamata: Gekkota: Carphodactylidae), a Member of the Ancient Gecko Lineage , 2014, Cytogenetic and Genome Research.

[50]  A. Fujiyama,et al.  Sex Chromosome Turnover Contributes to Genomic Divergence between Incipient Stickleback Species , 2014, PLoS genetics.

[51]  V. P. Margarido,et al.  Origin of the X1X1X2X2/X1X2Y sex chromosome system of Harttia punctata (Siluriformes, Loricariidae) inferred from chromosome painting and FISH with ribosomal DNA markers , 2014, Genetica.

[52]  T. Liehr,et al.  Comparative Chromosomal Mapping of Microsatellites in Leporinus Species (Characiformes, Anostomidae): Unequal Accumulation on the W Chromosomes , 2013, Cytogenetic and Genome Research.

[53]  K. Ocalewicz.  Telomeres in Fishes , 2013, Cytogenetic and Genome Research.

[54]  D. A. Martí,et al.  Tracking the evolution of sex chromosome systems in Melanoplinae grasshoppers through chromosomal mapping of repetitive DNA sequences , 2013, BMC Evolutionary Biology.

[55]  V. Trifonov,et al.  Independent Sex Chromosome Evolution in Lower Vertebrates: A Molecular Cytogenetic Overview in the Erythrinidae Fish Family , 2013, Cytogenetic and Genome Research.

[56]  M. Hedin,et al.  Evolution of karyotype, sex chromosomes, and meiosis in mygalomorph spiders (Araneae: Mygalomorphae) , 2013 .

[57]  E. Feldberg,et al.  Differentiation and evolutionary relationships in Erythrinus erythrinus (Characiformes, Erythrinidae): comparative chromosome mapping of repetitive sequences , 2013, Reviews in Fish Biology and Fisheries.

[58]  M. Dalíková,et al.  Neo-sex chromosomes and adaptive potential in tortricid pests , 2013, Proceedings of the National Academy of Sciences.

[59]  Bao Lou,et al.  Isolation and Characterization of Male-Specific DNA Markers in the Rock Bream Oplegnathus fasciatus , 2013, Marine Biotechnology.

[60]  Bao Lou,et al.  Chromosomal mapping of microsatellite repeats in the rock bream fish Oplegnathus fasciatus, with emphasis of their distribution in the neo-Y chromosome , 2013, Molecular Cytogenetics.

[61]  D. Blanco,et al.  The role of the Robertsonian rearrangements in the origin of the XX/XY1Y2 sex chromosome system and in the chromosomal differentiation in Harttia species (Siluriformes, Loricariidae) , 2013, Reviews in Fish Biology and Fisheries.

[62]  Heini M. Natri,et al.  Progressive Recombination Suppression and Differentiation in Recently Evolved Neo-sex Chromosomes , 2013, Molecular biology and evolution.

[63]  D. Bachtrog,et al.  Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration , 2013, Nature Reviews Genetics.

[64]  S. Brenner,et al.  A Trans-Species Missense SNP in Amhr2 Is Associated with Sex Determination in the Tiger Pufferfish, Takifugu rubripes (Fugu) , 2012, PLoS genetics.

[65]  M. Cioffi,et al.  Chromosomal distribution and evolution of repetitive DNAs in fish. , 2012, Genome dynamics.

[66]  M. Ferguson-Smith,et al.  Conservation of chromosomes syntenic with avian autosomes in squamate reptiles revealed by comparative chromosome painting , 2012, Chromosoma.

[67]  V. Nogaroto,et al.  Differentiation of repetitive DNA sites and sex chromosome systems reveal closely related group in Parodontidae (Actinopterygii: Characiformes) , 2011, Genetica.

[68]  E. Kejnovský,et al.  Microsatellite distribution on sex chromosomes at different stages of heteromorphism and heterochromatinization in two lizard species (Squamata: Eublepharidae: Coleonyx elegans and Lacertidae: Eremias velox) , 2011, BMC Genetics.

[69]  V. Trifonov,et al.  Whole chromosome painting reveals independent origin of sex chromosomes in closely related forms of a fish species , 2011, Genetica.

[70]  C. Peichel,et al.  Turnover of sex chromosomes and speciation in fishes , 2011, Environmental Biology of Fishes.

[71]  K. Sahara,et al.  Sex-Linked Pheromone Receptor Genes of the European Corn Borer, Ostrinia nubilalis, Are in Tandem Arrays , 2011, PloS one.

[72]  C. Moysés,et al.  Independent fusions and recent origins of sex chromosomes in the evolution and diversification of glass knife fishes (Eigenmannia) , 2011, Heredity.

[73]  C. Bidau,et al.  Sex and Neo-Sex Chromosomes in Orthoptera: A Review* , 2010 .

[74]  M. Cioffi,et al.  Initial steps in XY chromosome differentiation in Hoplias malabaricus and the origin of an X1X2Y sex chromosome system in this fish group , 2010, Heredity.

[75]  V. B. Kaiser,et al.  Evolution of sex chromosomes in insects. , 2010, Annual review of genetics.

[76]  L. Bertollo,et al.  Repetitive DNAs and Differentiation of Sex Chromosomes in Neotropical Fishes , 2010, Cytogenetic and Genome Research.

[77]  M. Cioffi,et al.  Chromosome spreading of associated transposable elements and ribosomal DNA in the fish Erythrinus erythrinus. Implications for genome change and karyoevolution in fish , 2010, BMC Evolutionary Biology.

[78]  D. Soltis,et al.  Review of the Application of Modern Cytogenetic Methods (FISH/GISH) to the Study of Reticulation (Polyploidy/Hybridisation). , 2010, Genes.

[79]  L. Rebordinos,et al.  Differentiation of the XY Sex Chromosomes in the Fish Hoplias malabaricus (Characiformes, Erythrinidae): Unusual Accumulation of Repetitive Sequences on the X Chromosome , 2010, Sexual Development.

[80]  B. Vyskot,et al.  New Horizons of Genomic in situ Hybridization , 2010, Cytogenetic and Genome Research.

[81]  D. Absher,et al.  A role for a neo-sex chromosome in stickleback speciation , 2009, Nature.

[82]  D. Filatov,et al.  Evolution of Neo-Sex Chromosomes in Silene diclinis , 2009, Genetics.

[83]  M. Cioffi,et al.  Chromosomal Variability among Allopatric Populations of Erythrinidae Fish Hoplias malabaricus: Mapping of Three Classes of Repetitive DNAs , 2009, Cytogenetic and Genome Research.

[84]  E. Kejnovský,et al.  The role of repetitive DNA in structure and evolution of sex chromosomes in plants , 2009, Heredity.

[85]  M. Ferguson-Smith,et al.  Neo-XY body: an analysis of XY1Y2 meiotic behavior in Carollia (Chiroptera, Phyllostomidae) by chromosome painting , 2009, Cytogenetic and Genome Research.

[86]  E. Kejnovský,et al.  Accumulation of Y-specific satellite DNAs during the evolution of Rumex acetosa sex chromosomes , 2009, Molecular Genetics and Genomics.

[87]  M. Shapiro,et al.  Turnover of Sex Chromosomes in the Stickleback Fishes (Gasterosteidae) , 2009, PLoS genetics.

[88]  M. Ferguson-Smith,et al.  Non-homologous sex chromosomes in two species of the genus Eigenmannia (Teleostei: Gymnotiformes) , 2008, Cytogenetic and Genome Research.

[89]  E. Kejnovský,et al.  Microsatellite accumulation on the Y chromosome in Silene latifolia. , 2008, Genome.

[90]  M. Ferguson-Smith,et al.  Mammalian karyotype evolution , 2007, Nature Reviews Genetics.

[91]  A. Vogler,et al.  Evolutionary dynamics of autosomal-heterosomal rearrangements in a multiple-X chromosome system of tiger beetles (Cicindelidae) , 2007, BMC Evolutionary Biology.

[92]  C. Martins,et al.  Identification of a new repetitive element in the sex chromosomes of Leporinus elongatus (Teleostei: Characiformes: Anostomidae): new insights into the sex chromosomes of Leporinus , 2007, Cytogenetic and Genome Research.

[93]  C. Martins.  Chromosomes and Repetitive DNAs: A Contribution to the Knowledge of the Fish Genome , 2007 .

[94]  J. Mank,et al.  Phylogenetic conservation of chromosome numbers in Actinopterygiian fishes , 2006, Genetica.

[95]  Fengtang Yang,et al.  Chromosome localization of microsatellite markers in the shrews of the Sorex araneus group , 2006, Chromosome Research.

[96]  A. Georges,et al.  The dragon lizard Pogona vitticeps has ZZ/ZW micro-sex chromosomes , 2005, Chromosome Research.

[97]  B. Teh,et al.  Genome-wide screening using array-CGH does not reveal microdeletions/microduplications in children with Kabuki syndrome , 2005, European Journal of Human Genetics.

[98]  J. Graves,et al.  Resolution and evolution of the duck-billed platypus karyotype with an X1Y1X2Y2X3Y3X4Y4X5Y5 male sex chromosome constitution. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[99]  Y. Tateno,et al.  Highly differentiated and conserved sex chromosome in fish species (Aulopus japonicus: Teleostei, Aulopidae). , 2003, Gene.

[100]  K. Gharbi,et al.  Comparative genome analysis of the primary sex-determining locus in salmonid fishes. , 2003, Genome research.

[101]  R. Devlin,et al.  Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences , 2002 .

[102]  T. Otto,et al.  Molecular differentiation of sex chromosomes probed by comparative genomic hybridization , 1999, Chromosoma.

[103]  J. Wall,et al.  Inbreeding, heterozygote advantage and the evolution of neo–X and neo–Y sex chromosomes , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[104]  P. Slijepcevic.  Telomeres and mechanisms of Robertsonian fusion , 1998, Chromosoma.

[105]  R. O’Neill,et al.  Comparative chromosome painting between two marsupials : origins of an XX/XY1Y2 sex chromosome system , 1997 .

[106]  K. Reed,et al.  Polymorphism of the nucleolus organizer region (NOR) on the putative sex chromosomes of Arctic char (Salvelinus alpinus) is not sex related , 1997, Chromosome Research.

[107]  R. Wing,et al.  A rapid procedure for the isolation of C0t-1 DNA from plants. , 1997, Genome.

[108]  G. Karpen,et al.  Drosophila ribosomal RNA genes function as an X-Y pairing site during male meiosis , 1990, Cell.

[109]  Robert J. Baker,et al.  Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes , 1990, Chromosoma.

[110]  A. T. Sumner.  A simple technique for demonstrating centromeric heterochromatin. , 1972, Experimental cell research.

[111]  I. Sampaio,et al.  First Report of Sex Chromosomes in Achiridae (Teleostei: Pleuronectiformes) with Inferences About the Origin of the Multiple X1X1X2X2/X1X2Y System and Dispersal of Ribosomal Genes in Achirus achirus. , 2017, Zebrafish.

[112]  E. Feldberg,et al.  Cytogenetic Diversity and the Evolutionary Dynamics of rDNA Genes and Telomeric Sequences in the Ancistrus Genus (Loricariidae: Ancistrini). , 2016, Zebrafish.

[113]  O. Moreira-Filho,et al.  Direct Chromosome Preparation from Freshwater Teleost Fishes , 2015 .

[114]  E. Feldberg,et al.  New Approach Data in Electric Fish ( Teleostei : Gymnotus ) : Sex Chromosome Evolution and Repetitive DNA , 2014 .

[115]  N. Carter,et al.  Generation of Paint Probes by Flow-Sorted and Microdissected Chromosomes , 2009 .

[116]  H. Ohtani,et al.  The ZZ/ZW sex-determining mechanism originated twice and independently during evolution of the frog, Rana rugosa , 2008, Heredity.

[117]  E. Garcia-Vazquez,et al.  Chromosomal mapping and nucleotide sequence of two tandem repeats of Atlantic salmon 5S rDNA. , 1994, Cytogenetics and cell genetics.

[118]  P. M. Galetti,et al.  Distribution of sex chromosome mechanisms in neotropical fish and description of a ZZ/ZW system in Parodon hilarii (Parodontidae) , 1993 .

[119]  O. M. Filho,et al.  Evidences for a multiple sex chromosome system with female heterogamety in Apareiodon affinis (Pisces, Parodontidae) , 1980 .