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Chromosomal Evolution in Lower Vertebrates: Sex Chromosomes in Neotropical Fishes

. 2017 Oct 05 ; 8 (10) : . [epub] 20171005

Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic

Document type Journal Article, Review

Abstract: Fishes exhibit the greatest diversity of species among vertebrates, offering a number of relevant models for genetic and evolutionary studies. The investigation of sex chromosome differentiation is a very active and striking research area of fish cytogenetics, as fishes represent one of the most vital model groups. Neotropical fish species show an amazing variety of sex chromosome systems, where different stages of differentiation can be found, ranging from homomorphic to highly differentiated sex chromosomes. Here, we draw attention on the impact of recent developments in molecular cytogenetic analyses that helped to elucidate many unknown questions about fish sex chromosome evolution, using excellent characiform models occurring in the Neotropical region, namely the Erythrinidae family and the Triportheus genus. While in Erythrinidae distinct XY and/or multiple XY-derived sex chromosome systems have independently evolved at least four different times, representatives of Triportheus show an opposite scenario, i.e., highly conserved ZZ/ZW system with a monophyletic origin. In both cases, recent molecular approaches, such as mapping of repetitive DNA classes, comparative genomic hybridization (CGH), and whole chromosome painting (WCP), allowed us to unmask several new features linked to the molecular composition and differentiation processes of sex chromosomes in fishes.

See more in PubMed

Ohno S. Sex Chromosomes and Sex-Linked Genes. Springer-Verlag; New York, NY, USA: 1967. p. 185.

Charlesworth D., Charlesworth B., Marais G. Steps in the evolution of heteromorphic sex chromosomes. Heredity. 2005;95:118–128. doi: 10.1038/sj.hdy.6800697. PubMed DOI

Steinemann S., Steinemann M. Retroelements: Tools for sex chromosome evolution. Cytogenet. Genome Res. 2005;110:134–143. doi: 10.1159/000084945. PubMed DOI

Bachtrog D. A dynamic view of sex chromosome evolution. Curr. Opin. Genet. Dev. 2006;16:578–585. doi: 10.1016/j.gde.2006.10.007. PubMed DOI

Graves J.A.M. Weird animal genomes and the evolution of vertebrate sex and sex chromosomes. Annu. Rev. Genet. 2008;42:565–586. doi: 10.1146/annurev.genet.42.110807.091714. PubMed DOI

Wright A.E., Dean R., Zimmer F., Mank J.E. How to make a sex chromosome. Nat. Commun. 2016;7 doi: 10.1038/ncomms12087. PubMed DOI PMC

Schartl M., Schmid M., Nanda I. Dynamics of vertebrate sex chromosome evolution: From equal size to giants and dwarfs. Chromosoma. 2016;125:553–571. doi: 10.1007/s00412-015-0569-y. PubMed DOI

Almeida-Toledo L.F., Foresti F. Morphologically differentiated sex chromosomes in neotropical freshwater fish. Genetica. 2001;111:91–100. doi: 10.1023/A:1013768104422. PubMed DOI

Cioffi M.B., Camacho J.P.M., Bertollo L.A.C. Repetitive DNAs and differentiation of sex chromosomes in neotropical fishes. Cytogenet. Genome Res. 2011;132:188–194. doi: 10.1159/000321571. PubMed DOI

Cioffi M.B., Moreira-Filho O., Almeida-Toledo L.F., Bertollo L.A.C. The contrasting role of heterochromatin in the differentiation of sex chromosomes: An overview from Neotropical fishes. J. Fish Biol. 2012;80:2125–2139. doi: 10.1111/j.1095-8649.2012.03272.x. PubMed DOI

Mank J.E., Avise J.C. Evolutionary diversity and turn-over of sex determination in teleost fishes. Sex. Dev. 2009;3:60–67. doi: 10.1159/000223071. PubMed DOI

Devlin R.H., Nagahama Y. Sex determination and sex differentiation in fish: An overview of genetic, physiological, and environmental influences. Aquaculture. 2002;208:191–364. doi: 10.1016/S0044-8486(02)00057-1. DOI

Oliveira C., Almeida-Toledo L.F., Foresti F. Karyotypic evolution in Neotropical fishes. In: Pisano E., Ozouf-Costaz C., Foresti F., Kapoor B.G., editors. Fish Cytogenetics. Science Publishers; Enfield, NH, USA: 2007. pp. 111–164.

Froese R., Pauly D., editors. FishBase. World Wide Web Electronic Publication. [(accessed on 2 February 2017)]; Available online: www.fishbase.org.

Kitano J., Peichel C.L. Turnover of sex chromosomes and speciation in fishes. Environ. Biol. Fishes. 2012;94:549–558. doi: 10.1007/s10641-011-9853-8. PubMed DOI PMC

Ferreira M., Garcia C., Matoso D.A., de Jesus I.S., Feldberg E. A new multiple sex chromosome system X1X1X2X2/X1Y1X2Y2 in Siluriformes: Cytogenetic characterization of Bunocephalus coracoideus (Aspredinidae) Genetica. 2016;144:591–599. doi: 10.1007/s10709-016-9927-9. PubMed DOI

Oliveira C., Foresti F., Hilsdorf A.W.S. Genetics of neotropical fish: From chromosomes to populations. Fish Physiol. Biochem. 2009;35:81–100. doi: 10.1007/s10695-008-9250-1. PubMed DOI

Arai R. Fish Karyotypes: A Check List. 1st ed. Springer; Tokyo, Japan: 2011. p. 340.

Parise-Maltempi P.P., Martins C., Oliveira C., Foresti F. Identification of a new repetitive element in the sex chromosomes of Leporinus elongatus (Teleostei: Characiformes: Anostomidae): New insights into the sex chromosomes of Leporinus Cytogenet. Genome Res. 2007;116:218–223. doi: 10.1159/000098190. PubMed DOI

Oliveira R.R., Feldberg E., dos Anjos M.B., Zuanon J. Occurrence of multiple sexual chromosomes (XX/XY1Y2 and Z1Z1Z2Z2/Z1Z2W1W2) in catfishes of the genus Ancistrus (Siluriformes: Loricariidae) from the Amazon basin. Genetica. 2008;134:243–249. doi: 10.1007/s10709-007-9231-9. PubMed DOI

Araya-Jaime C., Mateussi N.T.B., Utsunomia R., Costa-Silva G.J., Oliveira C., Foresti F. ZZ/Z0: The new system of sex chromosomes in Eigenmannia aff. trilineata (Teleostei: Gymnotiformes: Sternopygidae) characterized by molecular cytogenetics and DNA barcoding. Zebrafish. 2017 doi: 10.1089/zeb.2017.1422. PubMed DOI

Woram R.A., Gharbi K., Sakamoto T., Hoyheim B., Holm L.-E., Naish K., McGowan C., Ferguson M.M., Phillips R.B., Stein J., et al. Comparative genome analysis of the primary sex-determining locus in salmonid fishes. Genome Res. 2003;13:272–280. doi: 10.1101/gr.578503. PubMed DOI PMC

Mank J.E., Promislow D.E.L., Avise J.C. Evolution of alternative sex-determining mechanisms in teleost fishes. Biol. J. Linn. Soc. 2006;87:83–93. doi: 10.1111/j.1095-8312.2006.00558.x. DOI

Cioffi M.B., Molina W.F., Artoni R.F., Bertollo L.A.C. Chromosomes as tools for discovering biodiversity—The case of Erythrinidae fish family. In: Tirunilai P., editor. Recent Trends in Cytogenetic Studies—Methodologies and Applications. InTech Publisher; Rijeka, Croatia: 2012.

Cioffi M.B., Liehr T., Trifonov V., Molina W.F., Bertollo L.A.C. Independent sex chromosome evolution in lower vertebrates: A molecular cytogenetic overview in the Erythrinidae fish family. Cytogenet. Genome Res. 2013;141:186–194. doi: 10.1159/000354039. PubMed DOI

Artoni R.F., Falcão J.N., Moreira-Filho O., Bertollo L.A.C. An uncommon condition for a sex chromosome system in Characidae fish. Distribution and differentiation of the ZZ/ZW system in Triportheus. Chromosome Res. 2001;9:449–456. doi: 10.1023/A:1011620226348. PubMed DOI

Yano C.F., Bertollo L.A.C., Liehr T., Troy W.P., Cioffi M.B. W Chromosome dynamics in Triportheus species (Characiformes, Triportheidae): An ongoing process narrated by repetitive sequences. J. Hered. 2016;107:342–348. doi: 10.1093/jhered/esw021. PubMed DOI PMC

Galetti P.M., Jr., Lima N.R.W., Venere P.C. A monophyletic ZW sex chromosome system in Leporinus (Anostomidae, Characiformes) Cytologia. 1995;60:375–382. doi: 10.1508/cytologia.60.375. DOI

Vicente V.E., Bertollo L.A.C., Valentini S.R., Moreira-Filho O. Origin and differentiation of sex chromosome system in Parodon hilarii (Pisces, Parodontidae). Satellite DNA, G and C-banding. Genetica. 2003;119:115–120. doi: 10.1023/A:1026082904672. PubMed DOI

Manchado M., Zuasti E., Cross I., Merlo A., Infante C., Rebordinos L. Molecular characterization and chromosomal mapping of the 5S rRNA gene in Solea senegalensis: A new linkage to the U1, U2, and U5 small nuclear RNA genes. Genome. 2006;49:79–86. doi: 10.1139/g05-068. PubMed DOI

Pansonato-Alves J.C., Serrano É.A., Utsunomia R., Scacchetti P.C., Oliveira C., Foresti F. Single origin of sex chromosomes and multiple origins of B chromosomes in fish genus Characidium. PLoS ONE. 2014;9:e107169. doi: 10.1371/journal.pone.0107169. PubMed DOI PMC

Pennell M.W., Kirkpatrick M., Otto S.P., Vamosi J.C., Peichel C.L., Valenzuela N., Kitano J. Y fuse? Sex chromosome fusions in fishes and reptiles. PLoS Genet. 2015;11:e1005237. doi: 10.1371/journal.pgen.1005237. PubMed DOI PMC

Abbott J.K., Nordén A.K., Hansson B. Sex chromosome evolution: Historical insights and future perspectives. Proc. Biol. Sci. 2017;284 doi: 10.1098/rspb.2016.2806. PubMed DOI PMC

Van Doorn G.S., Kirkpatrick M. Turnover of sex chromosomes induced by sexual conflict. Nature. 2007;449:909–912. doi: 10.1038/nature06178. PubMed DOI

Kikuchi K., Hamaguchi S. Novel sex-determining genes in fish and sex chromosome evolution. Dev. Dyn. 2013;242:339–353. doi: 10.1002/dvdy.23927. PubMed DOI

Pokorná M., Altmanová M., Kratochvíl L. Multiple sex chromosomes in the light of female meiotic drive in amniote vertebrates. Chromosome Res. 2014;22:35–44. doi: 10.1007/s10577-014-9403-2. PubMed DOI

Brykov V.A. Mechanisms of sex determination in fish: Evolutionary and practical aspects. Russ. J. Mar. Biol. 2014;40:407–417. doi: 10.1134/S1063074014060145. DOI

Bachtrog D., Mank J.E., Peichel C.L., Kirkpatrick M., Otto S.P., Ashman T.L., Hahn M.W., Kitano J., Mayrose I., Ming R., et al. Sex determination: Why so many ways of doing it? PLoS Biol. 2014;12:e1001899. doi: 10.1371/journal.pbio.1001899. PubMed DOI PMC

Martínez P., Viñas A.M., Sánchez L., Díaz N., Ribas L., Piferrer F. Genetic architecture of sex determination in fish: Applications to sex ratio control in aquaculture. Front. Genet. 2014;5:340. doi: 10.3389/fgene.2014.00340. PubMed DOI PMC

Henning F., Trifonov V., Ferguson-Smith M.A., Almeida-Toledo L.F. Non-homologous sex chromosomes in two species of the genus Eigenmannia (Teleostei: Gymnotiformes) Cytogenet. Genome Res. 2008;121:55–58. doi: 10.1159/000124382. PubMed DOI

Pazian M.F., Shimabukuro-Dias C.K., Pansonato-Alves J.C., Oliveira C., Foresti F. Chromosome painting of Z and W sex chromosomes in Characidium (Characiformes, Crenuchidae) Genetica. 2013;141:1–9. doi: 10.1007/s10709-013-9701-1. PubMed DOI

Yano C.F., Bertollo L.A.C., Ezaz T., Trifonov V., Sember A., Liehr T., Cioffi M.B. Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae) Heredity. 2017;118:276–283. doi: 10.1038/hdy.2016.83. PubMed DOI PMC

Bertollo L.A.C., Born G.G., Dergam J.A., Fenocchio A.S., Moreira-Filho O. A biodiversity approach in the neotropical Erythrinidae fish, Hoplias malabaricus. Karyotypic survey, geographic distribution of cytotypes and cytotaxonomic considerations. Chromosome Res. 2000;8:603–613. doi: 10.1023/A:1009233907558. PubMed DOI

Bertollo L.A.C. Chromosome evolution in the Neotropical Erythrinidae fish family: An overview. In: Pizano E., Ozouf-Costaz C., Foresti F., Kapoor B.G., editors. Fish Cytogenetics. Science Publishers; Enfield, NH, USA: 2007. pp. 195–211.

Freitas N.L., Al-Rikabi A.B.H., Bertollo L.A.C., Ezaz T., Yano C.F., Oliveira E.A., Hatanaka T., Cioffi M.B. Early stages of XY sex chromosomes differentiation in the fish Hoplias malabaricus (Characiformes, Erythrinidae) revealed by DNA repeats accumulation. Curr. Genomics. 2017;18 doi: 10.2174/1389202918666170711160528. PubMed DOI PMC

Oliveira E.A., Sember A., Bertollo L.A.C., Yano C.F., Ezaz T., Moreira-Filho O., Hatanaka T., Trifonov V., Liehr T., Ráb P., et al. Tracking the evolutionary pathway of sex chromosomes among fishes: Characterizing the unique XX/XY1Y2 system in Hoplias malabaricus (Teleostei, Characiformes) Chromosoma. 2017 Submitted. PubMed

Sember A., Bertollo L.A.C., Yano C.F., Hatanaka T., Ráb P., de Oliveira E.A., Cioffi M.B. Sex chromosome evolution and genomic divergence in the fish Hoplias malabaricus (Characiformes, Erythrinidae) Front. Genet. 2017 Submitted. PubMed PMC

Born G.G., Bertollo L.A.C. An XX/XY sex chromosome system in a fish species, Hoplias malabaricus, with a polymorphic NOR-bearing X chromosome. Chromosome Res. 2000;8:111–118. doi: 10.1023/A:1009238402051. PubMed DOI

Cioffi M.B., Martins C., Vicari M.R., Rebordinos L., Bertollo L.A.C. Differentiation of the XY sex chromosomes in the fish Hoplias malabaricus (Characiformes, Erythrinidae). Unusual accumulation of repetitive sequences on the X chromosome. Sex. Dev. 2010;4:176–185. doi: 10.1159/000309726. PubMed DOI

Cioffi M.B., Martins C., Bertollo L.A.C. Comparative chromosome mapping of repetitive sequences. Implications for genomic evolution in the fish, Hoplias malabaricus. BMC Genet. 2009;10:34. doi: 10.1186/1471-2156-10-34. PubMed DOI PMC

Cioffi M.B., Kejnovský E., Bertollo L.A.C. The chromosomal distribution of microsatellite repeats in the genome of the wolf fish Hoplias malabaricus, focusing on the sex chromosomes. Cytogenet. Genome Res. 2011;132:289–296. doi: 10.1159/000322058. PubMed DOI

Cioffi M.B., Sánchez A., Marchal J.A., Kosyakova N., Liehr T., Trifonov V., Bertollo L.A.C. Whole chromosome painting reveals independent origin of sex chromosomes in closely related forms of a fish species. Genetica. 2011;139:1065–1072. doi: 10.1007/s10709-011-9610-0. PubMed DOI

Cioffi M.B., Bertollo L.A.C. Initial steps in XY chromosome differentiation in Hoplias. malabaricus and the origin of an X1X2Y sex chromosome system in this fish group. Heredity. 2010;105:554–561. doi: 10.1038/hdy.2010.18. PubMed DOI

Bertollo L.A.C., Fontes M.S., Fenocchio A.S., Cano J. The X1X2Y sex chromosome system in the fish Hoplias. malabaricus. I. G-, C- and chromosome replication banding. Chromosome Res. 1997;5:493–499. doi: 10.1023/A:1018477232354. PubMed DOI

Bertollo L.A.C., Mestriner C.A. The X1X2Y sex chromosome system in the fish Hoplias. malabaricus (Pisces, Erythrinidae). II. Meiotic analyses. Chromosome Res. 1998;6:141–147. doi: 10.1023/A:1009243114124. PubMed DOI

Rosa R., Laforga Vanzela A.L., Rubert M., Martins-Santos I.C., Giuliano-Caetano L. Differentiation of Y chromosome in the X1X1X2X2/X1X2Y sex chromosome system of Hoplias malabaricus (Characiformes, Erythrinidae) Cytogenet. Genome Res. 2009;127:54–60. doi: 10.1159/000269736. PubMed DOI

Green J.E., Dalíková M., Sahara K., Marec F., Akam M. XX/XY system of sex determination in the geophilomorph centipede Strigamia maritima. PLoS ONE. 2016;11:e0150292. doi: 10.1371/journal.pone.0150292. PubMed DOI PMC

Bertollo L.A.C., Oliveira C., Molina W.F., Margarido V.P., Fontes M.S., Pastori M.C., Falcão J.N., Fenocchio A.S. Chromosome evolution in the erythrinid fish, Erythrinus erythrinus (Teleostei: Characiformes) Heredity. 2004;93:228–233. doi: 10.1038/sj.hdy.6800511. PubMed DOI

Cioffi M.B., Martins C., Bertollo L.A.C. Chromosome spreading of associated transposable elements and ribosomal DNA in the fish Erythrinus erythrinus. Implications for genome change and karyoevolution in fish. BMC Evol. Biol. 2010;10:271. doi: 10.1186/1471-2148-10-271. PubMed DOI PMC

Martins N.F., Bertollo L.A.C., Troy W.P., Feldberg E., Valentin F.C.S., Cioffi M.B. Differentiation and evolutionary relationships in Erythrinus erythrinus (Characiformes, Erythrinidae): Comparative chromosome mapping of repetitive sequences. Rev. Fish Biol. Fish. 2013;23:261–269. doi: 10.1007/s11160-012-9292-4. DOI

Cioffi M.B., Sánchez A., Marchal J.A., Kosyakova N., Liehr T., Trifonov V., Bertollo L.A.C. Cross-species chromosome painting tracks the independent origin of multiple sex chromosomes in two cofamiliar Erythrinidae fishes. BMC Evol. Biol. 2011;11:186. doi: 10.1186/1471-2148-11-186. PubMed DOI PMC

Oliveira C., Avelino G.S., Abe K.T., Mariguela T.C., Benine R.C., Ortí G., Vari R.P., Corrêa e Castro R.M. Phylogenetic relationships within the speciose family Characidae (Teleostei: Ostariophysi: Characiformes) based on multilocus analysis and extensive ingroup sampling. BMC Evol. Biol. 2011;11:275. doi: 10.1186/1471-2148-11-275. PubMed DOI PMC

Mariguela T.C., Roxo F.F., Foresti F., Oliveira C. Phylogeny and biogeography of Triportheidae (Teleostei: Characiformes) based on molecular data. Mol. Phylogenet. Evol. 2016;96:130–139. doi: 10.1016/j.ympev.2015.11.018. PubMed DOI

Malabarba M.C.S.L. Revision of the Neotropical genus Triportheus. Cope, 1872 (Characiformes: Characidae) Neotrop. Ichthyol. 2004;2:167–204. doi: 10.1590/S1679-62252004000400001. DOI

Prestes L., Mota Soares M.G., Silva F.R., Bittencourt M.M. Dynamic population from Triportheus albus, T. angulatus and T. auritus (Characiformes: Characidae) in Amazonian Central lakes. Biota Neotrop. 2010;10:177–181. doi: 10.1590/S1676-06032010000300020. DOI

Falcão J.N. Ph.D. Thesis. Universidade de São Paulo; Ribeirão Preto, SP, Brazil: 1988. Caracterização Cariotípica em Peixes do Gênero Triportheus (Teleostei, Characiformes, Characidae)

Bertollo L.A.C., Cavallaro Z.I.A. Highly differentiated ZZ/ZW sex chromosome system in a Characidae fish, Triportheus guentheri. Cytogenet. Genome Res. 1992;60:60–63. doi: 10.1159/000133296. PubMed DOI

Sanchez S., Jorge L.C. A new report of the ZZ/ZW sex chromosome system in the genus Triportheus. (Pisces, Triportheinae) Cytologia. 1999;64:395–400. doi: 10.1508/cytologia.64.395. DOI

Artoni R.F., Bertollo L.A.C. Evolutionary aspects of the ZZ/ZW sex chromosome system in the Characidae fish, genus Triportheus. A monophyletic state and NOR location on the W chromosome. Heredity. 2002;89:15–19. doi: 10.1038/sj.hdy.6800081. PubMed DOI

Nirchio M., Oliveira C., Ferreira I.A., Granado A., Ron E. Extensive polymorphism and chromosomal characteristics of ribosomal DNA in the characid fish Triportheus venezuelensis (Characiformes, Characidae) Genet. Mol. Biol. 2007;30:25–30. doi: 10.1590/S1415-47572007000100007. DOI

Diniz D., Laudicina A., Cioffi M.B., Bertollo L.A.C. Microdissection and whole chromosome painting. Improving sex chromosome analysis in Triportheus (Teleostei, Characiformes) Cytogenet. Genome Res. 2008;122:163–168. doi: 10.1159/000163094. PubMed DOI

Diniz D., Moreira-Filho O., Bertollo L.A.C. Molecular cytogenetics and characterization of a ZZ/ZW sex chromosome system in Triportheus nematurus (Characiformes, Characidae) Genetica. 2008;133:85–91. doi: 10.1007/s10709-007-9187-9. PubMed DOI

Diniz D., Laudicina A., Bertollo L.A.C. Chromosomal location of 18S and 5S rDNA sites in Triportheus fish species (Characiformes, Characidae) Genet. Mol. Biol. 2009;32:37–41. doi: 10.1590/S1415-47572009005000017. PubMed DOI PMC

Yano C.F., Poltronieri J., Bertollo L.A.C., Artoni R.F., Liehr T., Cioffi M.B. Chromosomal mapping of repetitive DNAs in Triportheus trifurcatus (Characidae, Characiformes): Insights into the differentiation of the Z and W chromosomes. PLoS ONE. 2014;9:e90946. doi: 10.1371/journal.pone.0090946. PubMed DOI PMC

Yano C.F., Bertollo L.A.C., Rebordinos L., Merlo M.A., Liehr T., Portela-Bens S. Evolutionary dynamics of rDNAs and U2 small nuclear DNAs in Triportheus (Characiformes, Triportheidae): High variability and particular syntenic organization. Zebrafish. 2017;14:146–154. doi: 10.1089/zeb.2016.1351. PubMed DOI

Marquioni V., Bertollo L.A.C., Diniz D., Cioffi M.B. Comparative chromosomal mapping in Triportheus fish species. Analysis of synteny between ribosomal genes. Micron. 2013;45:129–135. doi: 10.1016/j.micron.2012.11.008. PubMed DOI

Reed K.M., Phillips R.B. Polymorphism of the nucleolar organizer region (NOR) on the putative sex chromosomes of Arctic char (Salvelinus alpinus) is not sex related. Chromosome Res. 1997;5:221–227. doi: 10.1023/A:1018411417816. PubMed DOI

Kawai A., Nishida-Umehara C., Ishijima J., Tsuda Y., Ota H., Matsuda Y. Different origins of bird and reptile sex chromosomes inferred from comparative mapping of chicken Z-linked genes. Cytogenet. Genome Res. 2007;117:92–102. doi: 10.1159/000103169. PubMed DOI

Badenhorst D., Stanyon R., Engstrom T., Valenzuela N. A ZZ/ZW microchromosome system in the spiny softshell turtle, Apalone spinifera, reveals an intriguing sex chromosome conservation in Trionychidae. Chromosome Res. 2013;21:137–147. doi: 10.1007/s10577-013-9343-2. PubMed DOI

Gatto K.P., Busin C.S., Lourenço L.B. Unraveling the sex chromosome heteromorphism of the paradoxical frog Pseudis tocantins. PLoS ONE. 2016;11:e0156176. doi: 10.1371/journal.pone.0156176. PubMed DOI PMC

Kejnovský E., Michalovová M., Šteflová P., Kejnovská I., Manzano S., Hobza R., Kubát Z., Kovařík J., Jamilena M., Vyskot B. Expansion of microsatellites on evolutionary young Y chromosome. PLoS ONE. 2013;8:e45519. doi: 10.1371/journal.pone.0045519. PubMed DOI PMC

Cioffi M.B., Kejnovský E., Marquioni V., Poltronieri J., Molina W.F., Diniz D., Bertollo L.A.C. The key role of repeated DNAs in sex chromosome evolution in two fish species with ZW sex chromosome system. Mol. Cytogenet. 2012;5:28. doi: 10.1186/1755-8166-5-28. PubMed DOI PMC

Rodrigues A.S., Aline Souza Medrado A.S., Diniz D., Oliveira C., Affonso P.R.A.M. ZZ/ZW sex chromosome system in the endangered fish Lignobrycon myersi Miranda-Ribeiro, 1956 (Teleostei, Characiformes, Triportheidae) Comp. Cytogenet. 2016;10:245–254. doi: 10.3897/CompCytogen.v10i2.8435. PubMed DOI PMC

Terencio M.L., Schneider C.H., Gross M.C., Silva A.M., Feldberg E., Porto J.I.R. Comparative cytogenetics of Carnegiella marthae and Carnegiella strigata (Characiformes, Gasteropelecidae) and description of a ZZ/ZW sex chromosome system. Genet. Mol. Biol. 2008;31:231–234. doi: 10.1590/S1415-47572008000200011. DOI

Soares R.X., Bertollo L.A.C., Cioffi M.B., Costa G.W.W.F., Molina W.F. Chromosomal distribution of two multigene families and the unusual occurrence of an X1X1X2X2/X1X2Y sex chromosome system in the dolphinfish (Coryphaenidae): An evolutionary perspective. Genet. Mol. Res. 2014;13:2470–2479. doi: 10.4238/2014.April.3.19. PubMed DOI

Bitencourt J.A., Sampaio I., Ramos R.T.C., Vicari M.R., Affonso P.R.A.M. 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. Zebrafish. 2016;14:90–95. doi: 10.1089/zeb.2016.1333. PubMed DOI

Moreira-Filho O., Bertollo L.A.C., Galetti P.M., Jr. Distribution of sex chromosome mechanisms in neotropical fish and description of a ZZ/ZW system in Parodon hilarii (Parodontidae) Caryologia. 1993;46:115–125. doi: 10.1080/00087114.1993.10797253. DOI

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