BACKGROUND: Java combtail fish Belontia hasselti (Cuvier, 1831), a member of the Osphronemidae family, inhabits lakes and rivers throughout Southeast Asia and Sri Lanka. Previous cytogenetic research revealed it possesses a diploid chromosome number of 48 chromosomes with a female-heterogametic ZZ/ZW sex chromosome system, where the W chromosome is distinguishable as the only metacentric element in the complement. Female-heterogametic sex chromosome systems seem to be otherwise surprisingly rare in the highly diverse order Perciformes and, therefore, B. hasselti provides an important comparative model to evolutionary studies in this teleost lineage. To examine the level of sex chromosome differentiation in B. hasselti and the contribution of repetitive DNAs to this process we combined bioinformatic analyses with chromosomal mapping of selected repetitive DNA classes, and comparative genomic hybridization. RESULTS: By providing the first satellitome study in Perciformes, we herein identified 13 satellite DNA monomers in B. hasselti, suggesting a very low diversity of satDNA in this fish species. Using fluorescence in situ hybridization, we revealed detectable clusters on chromosomes only for four satellite DNA monomers. Together with the two mapped microsatellite motifs, the repeats primarily accumulated on autosomes, with no distinct clusters located on the sex chromosomes. Comparative genomic hybridization showed no region with accumulated female-specific or enriched repeats on the W chromosome. Telomeric repeats terminated all chromosomes, and no additional interstitial sites were detected. CONCLUSION: These data collectively indicate a low degree of sex chromosome differentiation in B. hasselti despite their considerable heteromorphy. Possible mechanisms that may underlie this pattern are discussed.

Departamento de Ciências Biológicas Faculdade de Ciências Universidade Estadual Paulista Bauru São Paulo 17033 360 Brazil

Departamento de Genética e Evolução Universidade Federal de São Carlos São Carlos São Paulo 13565 905 Brazil

Department of Biology Faculty of Science Khon Kaen University Muang Khon Kaen 40002 Thailand

Faculty of Interdisciplinary Studies Khon Kaen University Nong Khai Campus Muang Nong Khai 43000 Thailand

Jena University Hospital Friedrich Schiller University Institute of Human Genetics 07747 Jena Germany

Laboratory of Fish Genetics Institute of Animal Physiology and Genetics Czech Academy of Sciences Rumburská 89 Liběchov 277 21 Czech Republic

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Charlesworth D. When and how do sex-linked regions become sex chromosomes? Evolution. 2021; 10.1111/evo.14196 PubMed

Abbott JK, Nordén AK, Hansson B. Sex chromosome evolution: historical insights and future perspectives. Proc R Soc B. 2017. 10.1098/rspb.2016.2806. PubMed PMC

Vicoso B. Molecular and evolutionary dynamics of animal sex-chromosome turnover. Nat Ecol Evol. 2019. 10.1038/s41559-019-1050-8. PubMed DOI

Furman BL, Metzger DC, Darolti I, Wright AE, Sandkam BA, Almeida P, et al. Sex chromosome evolution: so many exceptions to the rules. Genome Biol Evol. 2020. 10.1093/gbe/evaa081. PubMed DOI PMC

Jay P, Jeffries D, Hartmann FE, Véber A, Giraud T. Why do sex chromosomes progressively lose recombination? Trends Genet. 2024. 10.1016/j.tig.2024.03.005. PubMed DOI

Saunders PA, Muyle A. Sex chromosome evolution: hallmarks and question marks. Mol Biol Evol. 2024. 10.1093/molbev/msae218. PubMed DOI PMC

Sember A, Nguyen P, Perez MF, Altmanová M, Ráb P, Cioffi MB. Multiple sex chromosomes in teleost fishes from a cytogenetic perspective: state of the art and future challenges. Phil Trans R Soc B: Biol Sci. 2021. 10.1098/rstb.2020.0098. PubMed DOI PMC

Lichilín N, Salzburger W, Böhne A. No evidence for sex chromosomes in natural populations of the cichlid fish PubMed DOI PMC

Smith SH, Hsiung K, Böhne A. Evaluating the role of sexual antagonism in the evolution of sex chromosomes: new data from fish. Curr Opin Genet Dev. 2023. 10.1016/j.gde.2023.102078. PubMed DOI

Kitano J, Ansai S, Takehana Y, Yamamoto Y. Diversity and convergence of sex-determination mechanisms in teleost fish. Annu Rev Anim Biosci. 2024. 10.1146/annurev-animal-021122-113935. PubMed DOI

Purcell CM, Seetharam AS, Snodgrass O, Ortega-García S, Hyde JR, Severin AJ. Insights into teleost sex determination from the PubMed DOI PMC

Koyama T, Nakamoto M, Morishima K, Yamashita R, Yamashita T, Sasaki K, et al. A SNP in a steroidogenic enzyme is associated with phenotypic sex in PubMed DOI

Li M, Xu X, Liu S, Fan G, Zhou Q, Chen S. The chromosome-level genome assembly of the Japanese yellowtail jack PubMed DOI

Gammerdinger WJ, Kocher TD. Unusual diversity of sex chromosomes in African cichlid fishes. Genes. 2018. 10.3390/genes9100480. PubMed DOI PMC

El Taher A, Ronco F, Matschiner M, Salzburger W, Böhne A. Dynamics of sex chromosome evolution in a rapid radiation of cichlid fishes. Sci Adv. 2021. 10.1126/sciadv.abe8215. PubMed DOI PMC

Bellafronte E, Schemberger MO, Artoni RF, Filho OM, Vicari MR. Sex chromosome system ZZ/ZW in PubMed DOI PMC

Schemberger MO, Oliveira JIN, Nogaroto V, Almeida MC, Artoni RF, Cestari MM, et al. Construction and characterization of a repetitive DNA library in Parodontidae (Actinopterygii: Characiformes): a genomic and evolutionary approach to the degeneration of the W sex chromosome. Zebrafish. 2014. 10.1089/zeb.2014.1013. PubMed DOI PMC

Schemberger MO, Nascimento VD, Coan R, Ramos É, Nogaroto V, Ziemniczak K, et al. DNA transposon invasion and microsatellite accumulation guide W chromosome differentiation in a Neotropical fish genome. Chromosoma. 2019. 10.1007/s00412-019-00721-9. PubMed DOI

Scacchetti PC, Utsunomia R, Pansonato-Alves JC, Vicari MR, Artoni RF, Oliveira C, et al. Chromosomal mapping of repetitive DNAs in PubMed DOI

Yano CF, Bertollo LAC, Ezaz T, Trifonov V, Sember A, Liehr T, et al. Highly conserved Z and molecularly diverged W chromosomes in the fish genus PubMed DOI PMC

de Barros CL, Piscor D, Parise-Maltempi PP, Feldberg E. Differentiation and evolution of the W chromosome in the fish species of PubMed DOI

Souza-Borges CHD, Utsunomia R, Varani AM, Uliano-Silva M, Lira LVG, Butzge AJ, et al. De novo assembly and characterization of a highly degenerated ZW sex chromosome in the fish PubMed DOI PMC

Wolf IR, Schemberger MO, Azambuja M, Oliveira FS, Nogaroto V, Valente GT, et al. The long-read assembly of PubMed DOI PMC

Jeffries DL, Mee JA, Peichel CL. Identification of a candidate sex determination gene in PubMed DOI PMC

Teal CN, Coykendall DK, Campbell MR, Eardley DL, Delomas TA, Shira JT, et al. Sex-specific markers undetected in green sunfish PubMed DOI

Dass CC. Cited in Rishi KK. Current status of fish cytogenetics. In: Das and Jhingram, editors, Fish Genetics in India, Proc. 70th Indian Sci. Cong. vol. 2. Today and Tomorrow’s Printers; 1983. p. 1.

Chaiyasan P, Mingkwan B, Jantarat S, Suwannapoom C, Cioffi MB, Liehr T, et al. Classical and molecular cytogenetics of DOI

Nelson JS, Grande TC, Wilson MVH. Fishes of the world. Hoboken: Wiley; 2016.

Roberts TR. The freshwater fishes of Western Borneo (Kalimantan Barat, Indonesia). Memoirs of the California Academy of Sciences; 1989.

Pethiyagoda R. Conservation of Sri Lankan freshwater fishes. The fauna of Sri Lanka; 2006. pp. 103–12.

Terencio ML, Schneider CH, Gross MC, Vicari MR, Farias IP, Passos KB, et al. Evolutionary dynamics of repetitive DNA in PubMed DOI

Poltronieri J, Marquioni V, Bertollo LAC, Kejnovsky E, Molina WF, Liehr T, et al. Comparative chromosomal mapping of microsatellites in PubMed DOI

Ziemniczak K, Traldi JB, Nogaroto V, Almeida MC, Artoni RF, Moreira-Filho O, et al. PubMed DOI

Yano CF, Bertollo LAC, Liehr T, Troy WP, Cioffi MB. W chromosome dynamics in PubMed DOI PMC

Dulz TA, Azambuja M, Lorscheider CA, Noleto RB, Moreira-Filho O, Nogaroto V, et al. Repetitive DNAs and chromosome evolution in PubMed DOI

Ota K, Tateno Y, Gojobori T. Highly differentiated and conserved sex chromosome in fish species ( PubMed DOI

Yano CF, Sember A, Kretschmer R, Bertollo LAC, Ezaz T, Hatanaka T, et al. Against the mainstream: exceptional evolutionary stability of ZW sex chromosomes across the fish families Triportheidae and Gasteropelecidae (Teleostei: Characiformes). Chromosome Res. 2021. 10.1007/s10577-021-09674-1. PubMed DOI

Nirchio M, Oliveira C, Cioffi MB, Rossi FMC, Valdiviezo J, Paim FG et al. Occurrence of sex chromosomes in fish of the genus PubMed PMC

Nanda I, Volff JN, Weis S, Körting C, Froschauer A, Schmid M, et al. Amplification of a long terminal repeat-like element on the Y chromosome of the platyfish, PubMed DOI

Terencio ML, Schneider CH, Gross MC, Nogaroto V, Almeida MC, Artoni RF, et al. Repetitive sequences associated with differentiation of W chromosome in PubMed DOI

Chalopin D, Volff JN, Galiana D, Anderson JL, Schartl M. Transposable elements and early evolution of sex chromosomes in fish. Chromosome Res. 2015. 10.1007/s10577-015-9490-8. PubMed DOI

Utsunomia R, Silva DMZA, Ruiz-Ruano FJ, Goes CAG, Melo S, Ramos LP, et al. Satellitome landscape analysis of PubMed DOI PMC

Kretschmer R, Goes CAG, Bertollo LAC, Ezaz T, Porto-Foresti F, Toma GA, et al. Satellitome analysis illuminates the evolution of ZW sex chromosomes of Triportheidae fishes (Teleostei: Characiformes). Chromosoma. 2022. 10.1007/s00412-022-00768-1. PubMed DOI

Štundlová J, Hospodářská M, Lukšíková K, Voleníková A, Pavlica T, Altmanová M, et al. Sex chromosome differentiation via changes in the Y chromosome repeat landscape in African annual killifishes PubMed DOI

de Moraes RLR, Sassi FMC, Vidal JAD, Goes CAG, Santos RZ, Stornioli JHF, et al. Chromosomal rearrangements and satellite DNAs: extensive chromosome reshuffling and the evolution of neo-sex chromosomes in the genus PubMed DOI PMC

Lukšíková K, Pavlica T, Altmanová M, Štundlová J, Pelikánová Š, Simanovsky SA, et al. Conserved satellite DNA motif and lack of interstitial telomeric sites in highly rearranged African PubMed DOI

Deon GA, dos Santos RZ, Sassi FDMC, Moreira-Filho O, Vicari MR, Porto-Foresti F, et al. The role of satellite DNAs in the chromosomal rearrangements and the evolution of the rare XY PubMed DOI

Toma GA, Sember A, Goes CAG, Kretschmer R, Porto-Foresti F, Bertollo LAC, et al. Satellite DNAs and the evolution of the multiple X PubMed DOI PMC

Herpin A, Braasch I, Kraeussling M, Schmidt C, Thoma EC, Nakamura S, et al. Transcriptional rewiring of the sex determining PubMed DOI PMC

Schartl M, Schories S, Wakamatsu Y, Nagao Y, Hashimoto H, Bertin C, et al. PubMed DOI PMC

Wang L, Sun F, Wan Z, Yang Z, Tay YX, Lee M, et al. Transposon-induced epigenetic silencing in the X chromosome as a novel form of PubMed DOI PMC

Bertho S, Herpin A, Schartl M, Guiguen Y. Lessons from an unusual vertebrate sex-determining gene. Phil Trans R Soc B: Biol Sci. 2021. 10.1098/rstb.2020.0092. PubMed DOI PMC

Plohl M, Meštrović N, Mravinac B. Satellite DNA Evolution. PubMed

Garrido-Ramos MA, Satellite DNA: an evolving topic. Genes. 2017. 10.3390/genes8090230. PubMed PMC

Šatović-Vukšić E, Plohl M. Satellite DNAs– from localized to highly dispersed genome components. Genes. 2023. 10.3390/genes14030742. PubMed DOI PMC

Crepaldi C, Parise-Maltempi PP. Heteromorphic sex chromosomes and their DNA content in fish: an insight through satellite DNA accumulation in PubMed DOI

de Oliveira MPB, Kretschmer R, Deon GA, Toma GA, Ezaz T, Goes CAG, et al. Following the pathway of W chromosome differentiation in PubMed DOI PMC

Crepaldi C, Martí E, Gonçalves ÉM, Martí DA, Parise-Maltempi PP. Genomic differences between the sexes in a fish species seen through satellite DNAs. Front Genet. 2021. 10.3389/fgene.2021.728670. PubMed DOI PMC

Toma GA, dos Santos N, dos Santos R, Rab P, Kretschmer R, Ezaz T, et al. Cytogenetics meets genomics: cytotaxonomy and genomic relationships among color variants of the Asian arowana PubMed DOI PMC

Ruiz-Ruano F, López-León M, Cabrero J, Camacho JPM. High-throughput analysis of the satellitome illuminates satellite DNA evolution. Sci Rep. 2016. 10.1038/srep28333. PubMed DOI PMC

Bardella VB, Milani D, Cabral-de-Mello DC. Analysis of PubMed DOI

Cabral-de-Mello DC, Marec F. Universal fluorescence PubMed DOI

Stornioli JHF, Goes CAG, Calegari RM, dos Santos RZ, Giglio LM, Foresti F, et al. The B chromosomes of PubMed DOI PMC

Voleníková A, Lukšíková K, Mora P, Pavlica T, Altmanová M, Štundlová J, et al. Fast satellite DNA evolution in PubMed DOI PMC

Silva DMZA, Utsunomia R, Ruiz-Ruano FJ, Daniel SN, Porto-Foresti F, Hashimoto DT, et al. High-throughput analysis unveils a highly shared satellite DNA library among three species of fish genus PubMed DOI PMC

Serrano-Freitas ÉA, Silva DMZA, Ruiz-Ruano FJ, Utsunomia R, Araya-Jaime C, Oliveira C, et al. Satellite DNA content of B chromosomes in the characid fish PubMed DOI

Biscotti MA, Olmo E, Heslop-Harrison JS. Repetitive DNA in eukaryotic genomes. Chromosome Res. 2015. 10.1007/s10577-015-9499-z. PubMed DOI

Camacho JPM, Cabrero J, Lopez-Leon MD, Martín-Peciña M, Perfectti F, Garrido-Ramos MA, et al. Satellitome comparison of two oedipodine grasshoppers highlights the contingent nature of satellite DNA evolution. BMC Biol. 2022. 10.1186/s12915-021-01216-9. PubMed DOI PMC

Schartl M, Schmid M, Nanda I. Dynamics of vertebrate sex chromosome evolution: from equal size to giants and dwarfs. Chromosoma. 2016. 10.1007/s00412-015-0569-y. PubMed DOI

Müller S, Du K, Guiguen Y, Pichler M, Nakagawa S, Stöck M, et al. Massive expansion of sex-specific SNPs, transposon-related elements, and neocentromere formation shape the young W-chromosome from the mosquitofish PubMed PMC

Voleníková AC, Sahara K, Štundlová J, Dalíková M, Koutecký P, Grof-Tisza P, et al. Ghost W chromosomes and unique genome architecture in ghost moths of the family Hepialidae. bioRxiv. 2023. 10.1101/2023.09.03.556148. DOI

Soh YS, Alföldi J, Pyntikova T, Brown LG, Graves T, Minx PJ, et al. Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes. Cell. 2014. 10.1016/j.cell.2014.09.052. PubMed DOI PMC

Bachtrog D, Mahajan S, Bracewell R. Massive gene amplification on a recently formed PubMed DOI PMC

Vegesna R, Tomaszkiewicz M, Ryder OA, Campos-Sánchez R, Medvedev P, DeGiorgio M, et al. Ampliconic genes on the great ape Y chromosomes: rapid evolution of copy number but conservation of expression levels. Genome Biol Evol. 2020. 10.1093/gbe/evaa088. PubMed DOI PMC

Zhou R, Macaya-Sanz D, Carlson CH, Schmutz J, Jenkins JW, Kudrna D, et al. A willow sex chromosome reveals convergent evolution of complex palindromic repeats. Genome Biol. 2020. 10.1186/s13059-020-1952-4. PubMed DOI PMC

Conte MA, Clark FE, Roberts RB, Xu L, Tao W, Zhou Q, et al. Origin of a giant sex chromosome. Mol Biol Evol. 2021. 10.1093/molbev/msaa319. PubMed DOI PMC

Rejón CR, Jamilena M, Garrido Ramos M, Parker JS, Ruiz Rejón M. Cytogenetic and molecular analysis of the multiple sex chromosome system of DOI

Mestriner CA, Galetti PM, Valentini SR, Ruiz IRG, Abel LDS, Moreira-Filho O, et al. Structural and functional evidence that a B chromosome in the characid fish PubMed DOI

Artoni RF, Vicari MR, Endler AL, Cavallaro ZI, de Jesus CM, Almeida MC, et al. Banding pattern of A and B chromosomes of PubMed DOI

Poletto AB, Ferreira IA, Martins C. The B chromosomes of the African cichlid fish PubMed DOI PMC

dos Santos LP, Francisco CM, Campos Júnior EO, Castro JP, Utsunomia R, Morelli S, et al. Chromosomal instability and origin of B chromosomes in the Amazonian glass tetra PubMed DOI

Kasiroek W, Indananda C, Luangoon N, Pinthong K, Supiwong W, Tanomtong A. First chromosome analysis of the humpback cardinalfish, DOI

Supiwong W, Tanomtong A, Pinthong K, Kaewmad P, Poungnak P, Jangsuwan N. The first chromosomal characteristics of nucleolar organizer regions and karyological analysis of Pink anemonefish, DOI

Sumner AT. A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res. 1972. 10.1016/0014-4827(72)90558-7. PubMed DOI

Sambrook J, Russel DW. Molecular cloning: a laboratory manual. Cold Spring Harbor; 2001.

Novák P, Robledillo LA, Koblížková A, Vrbová I, Neumann P, Macas J. TAREAN: a computational tool for identification and characterization of satellite DNA from unassembled short reads. Nucleic Acids Res. 2017. 10.1093/nar/gkx257. PubMed DOI PMC

Bolger AM, Lohse M, Usadel B, Trimmomatic. A flexible trimmer for illumina sequence data. Bioinformatics. 2014. 10.1093/bioinformatics/btu170. PubMed PMC

Schmieder R, Edwards R. Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PLoS ONE. 2011. 10.1371/journal.pone.0017288. PubMed DOI PMC

Smit AFA, Hubley R, Green P. RepeatMasker Open-3.0 1996–2010. 2017.

Ijdo JW, Wells RA, Baldini A, Reeders ST. Improved telomere detection using a telomere repeat probe (TTAGGG) PubMed DOI PMC

Sassi FMC, Toma GA, Cioffi MB. FISH-in fish chromosomes. Cytogenetics and molecular cytogenetics. CRC: Boca Raton 2022. pp. 281–97.

Zwick MS, Hanson RE, Islam-Faridi MN, Stelly DM, Wing RA, Price HJ, et al. A rapid procedure for the isolation of PubMed DOI

Sember A, Bertollo LAC, Ráb P, Yano CF, Hatanaka T, Oliveira EA, et al. Sex chromosome evolution and genomic divergence in the fish PubMed DOI PMC