Osteoglossiformes represents one of the most ancestral teleost lineages, currently widespread over almost all continents, except for Antarctica. However, data involving advanced molecular cytogenetics or comparative genomics are yet largely limited for this fish group. Therefore, the present investigations focus on the osteoglossiform family Arapaimidae, studying a unique fish model group with advanced molecular cytogenetic genomic tools. The aim is to better explore and clarify certain events and factors that had impact on evolutionary history of this fish group. For that, both South American and African representatives of Arapaimidae, namely Arapaima gigas and Heterotis niloticus, were examined. Both species differed markedly by diploid chromosome numbers, with 2n = 56 found in A. gigas and 2n = 40 exhibited by H. niloticus. Conventional cytogenetics along with fluorescence in situ hybridization revealed some general trends shared by most osteoglossiform species analyzed thus far, such as the presence of only one chromosome pair bearing 18S and 5S rDNA sites and karyotypes dominated by acrocentric chromosomes, resembling thus the patterns of hypothetical ancestral teleost karyotype. Furthermore, the genomes of A. gigas and H. niloticus display remarkable divergence in terms of repetitive DNA content and distribution, as revealed by comparative genomic hybridization (CGH). On the other hand, genomic diversity of single copy sequences studied through principal component analyses (PCA) based on SNP alleles genotyped by the DArT seq procedure demonstrated a very low genetic distance between the South American and African Arapaimidae species; this pattern contrasts sharply with the scenario found in other osteoglossiform species. Underlying evolutionary mechanisms potentially explaining the obtained data have been suggested and discussed.

Departamento de Genética e Evolução Universidade Federal de São Carlos Rodovia Washington Luiz São Carlos SP Brazil

Department of Fisheries and Aquaculture Adamawa State University Adamawa State Nigeria

Institute for Applied Ecology University of Canberra Canberra Australia

Institute of Human Genetics University Hospital Jena Jena Germany

Instituto Nacional de Pesquisas da Amazônia Coordenação de Biodiversidade Laboratório de Genética Animal Petrópolis CEP Manaus AM Brazil

Laboratory of Fish Genetics Institute of Animal Physiology and Genetics Czech Academy of Sciences Czech Republic

Secretaria de Estado de Educação de Mato Grosso SEDUC MT Cuiabá MT Brazil

Toxic Substances in Livestock and Aquatic Animals Research Group KhonKaen University Muang KhonKaen Thailand

Zobrazit více v PubMed

Lundberg JG. African-South American freshwater fish clades and continental drift: problems with a paradigm In: Goldblatt P, editor. Biological relationships between Africa and South America. USA, Yale University Press; 1993. pp. 156–198.

Bǎnǎrescu P. Zoogeography of fresh waters Vol. 3, Distribution and dispersal of freshwater animals in Africa, Pacific areas and South America. Wiesbaden, Germany: AULA-Vlg; 1995.

Kumazawa Y, Nishida M. Molecular phylogeny of osteoglossoids: A new model for Gondwanian origin and plate tectonic transportation of the Asian arowana. Mol Biol Evol. 2000;17: 1869–1878. 10.1093/oxfordjournals.molbev.a026288 PubMed DOI

Wilson MVH, Murray AM. Osteoglossomorpha: phylogeny, biogeography, and fossil record and the significance of key African and Chinese fossil taxa. Geol Soc Spec Publ. 2008;295: 185–219.

Lavoué S. Was Gondwanan breakup the cause of the intercontinental distribution of Osteoglossiformes? A time-calibrated phylogenetic test combining molecular, morphological, and paleontological evidence. Mol Phylogenet Evol. 2016;99: 34–43. 10.1016/j.ympev.2016.03.008 PubMed DOI

Nelson JS, Grande TC, Wilson MVH. Fishes of the World John Wiley & Sons; 2016.

Betancur-R R, Wiley EO, Arratia G, Acero A, Bailly N, Miya M, et al. Phylogenetic classification of bony fishes. BMC Evol Biol. 2017;17: 162 10.1186/s12862-017-0958-3 PubMed DOI PMC

Mirande JM. Combined phylogeny of ray‐finned fishes (Actinopterygii) and the use of morphological characters in large‐scale analyses. Cladistics. 2017;33: 333–350. PubMed

Li G-Q, Wilson MVH. Phylogeny of osteoglossomorpha Interrelationships of fishes. Elsevier; 1996. pp. 163–174.

Adite A, Winemiller KO, Fiogbe ED. Ontogenetic, seasonal, and spatial variation in the diet of

Hurtado LA, Carrera E, Adite A, Winemiller KO. Genetic differentiation of a primitive teleost, the African bonytongue PubMed DOI

Mustapha MK.

Günther A. XV.—New fishes from the Gaboon and Gold Coast. Ann Mag Nat Hist. 1867;20: 110–117.

Stewart DJ. A New Species of

Stewart DJ. Re-description of

Reis RE, Albert JS, Di Dario F, Mincarone MM, Petry P, Rocha LA. Fish biodiversity and conservation in South America. J Fish Biol. 2016;89:12–47 10.1111/jfb.13016 PubMed DOI

Castello L. Nesting habitat of

McConnell R, Lowe-McConnell RH. Ecological studies in tropical fish communities Cambridge University Press; 1987.

Queiroz HL. Natural history and conservation of pirarucu, Àrapaima gigas', at the Amazonian Várzea: red giants in muddy waters. PhD dissertation. University of St Andrews. 2000. Available from: https://research-repository.st-andrews.ac.uk/handle/10023/2818

Monteiro LBB, Soares MDC, Catanho MTJ, Honczaryk A. Aspectos reprodutivos e perfil hormonal dos esteróides sexuais do pirarucu,

Gurdak DJ, Stewart DJ, Castello L, Arantes CC. Diversity in reproductive traits of arapaima (

Santos RS.

Lundberg JG, Chernoff B. A Miocene fossil of the amazonian fish

Gayet M, Meunier FJ. Maastrichtian to early late Paleocene freshwater Osteichthyes of Bolivia: additions and comments. Phylogeny Classif Neotrop Fishes. 1998; 85–110.

Taverne L. Les ostéoglossomorphes marins de l’Éocène du Monte Bolca (Italie): Monopteros Volta 1796, Thrissopterus Heckel, 1856 et Foreyichthys Taverne, 1979. Considérations sur la phylogénie des téléostéens ostéoglossomorphes. Stud e Ric sui Giacimenti Terziari di Bolca. 1998;7: 67–158.

Newbrey MG, Bozek MA. A new species of

Newbrey MG, Bozek MA. Age, growth, and mortality of

Pindell JL, Cande SC, Pitman WC III, Rowley DB, Dewey JF, LaBrecque J, et al. A plate-kinematic framework for models of Caribbean evolution. Tectonophysics. 1988;155: 121–138.

Rabinowitz PD, LaBrecque J. The Mesozoic South Atlantic Ocean and evolution of its continental margins. J Geophys Res. 1979;84: 5973.

Schueler MG, Higgins AW, Rudd MK, Gustashaw K, Willard H. Genomic and genetic definition of a functional human centromere. Science. 2001;294: 109–115. 10.1126/science.1065042 PubMed DOI

Biscotti MA, Olmo E, Heslop-Harrison JSP. Repetitive DNA in eukaryotic genomes. Chromosome Res. 2015;23: 415–20. 10.1007/s10577-015-9499-z PubMed DOI

Cioffi MB, Bertollo LAC. Chromosomal distribution and evolution of repetitive DNAs in fish In: Garrido R, editor. Repetitive DNAs genome dynamics. Basel: Karger; 2012. pp. 197–221. 10.1159/000337950 PubMed DOI

Ráb P, Yano CF, Lavoué S, Jegede OI, Bertollo LAC, Ezaz T, et al. Karyotype and mapping of repetitive DNAs in the African butterfly fish PubMed DOI

Marques DK, Venere PC, Galetti Junior PM. Chromosomal characterization of the bonytongue

Da Rosa R, Rubert M, Caetano-Filho M, Giuliano-Caetano L. Conserved cytogenetic features in the Amazonian Arapaima,

Kallioniemi A, Kallioniemi OP, Sudar D, Rutovitz D, Gray JW, Waldman F, et al. Comparative genomic hybridization for molecular cytogenetic analysis of solid tumors. Science. 1992;258: 818–821. PubMed

Lim KY, Kovarik A, Matyasek R, Chase MW, Clarkson JJ, Grandbastien MA, et al. Sequence of events leading to near‐complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol. 2007;175: 756–763. 10.1111/j.1469-8137.2007.02121.x PubMed DOI

Mahelka V, Kopecký D, Paštová L. On the genome constitution and evolution of intermediate wheatgrass ( PubMed DOI PMC

Symonová R, Sember A, Majtánová Z, Ráb P. Characterization of fish genomes by GISH and CGH Fish Cytogenet Tech Ray-Fin Fishes Chondrichthyans CCR Press Boca Rat; 2015; 118–131.

Kato A, Vega JM, Han F, Lamb JC, Birchler JA. Advances in plant chromosome identification and cytogenetic techniques. Curr Opin Plant Biol. 2005;8: 148–154. 10.1016/j.pbi.2005.01.014 PubMed DOI

Chester M, Leitch AR, Soltis PS, Soltis DE. Review of the application of modern cytogenetic methods (FISH/GISH) to the study of reticulation (polyploidy/hybridisation). Genes. 2010;1: 166–192. 10.3390/genes1020166 PubMed DOI PMC

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

Cavallini MM, Bertollo LAC. Indução de mitoses em

Bertollo LAC, Cioffi MB, Moreira-Filho O. Direct chromosome preparation from freshwater teleost fishes In: Ozouf-Costaz C, Pisano E, Foresti F, Almeida Toledo LF, editors. Fish cytogenetic techniques (Chondrichthyans and Teleosts). CRC Press: Enfield USA; 2015. pp.21–26.

Howell WM, Black DA. Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia. 1980;36: 1014–1015. PubMed

Schmid M. Chromosome banding in Amphibia. IV. Differentiation of GC-and AT-rich chromosome regions in Anura. Chromosoma. 1980;77: 83–103. PubMed

Sumner AT. A simple technique for demonstrating centromeric heterochromatin. Experimental Cell Research. 1972. 75: 304–306. PubMed

Martins C, Ferreira IA, Oliveira C, Foresti F, Galetti PM. A tandemly repetitive centromeric DNA sequence of the fish PubMed DOI

Cioffi MB, Martins C, Centofante L, Jacobina U, Bertollo LAC. Chromosomal variability among allopatric populations of Erythrinidae fish PubMed DOI

Pinkel D, Straume T, Gray J. Cytogenetic analysis using quantitative, high sensitivity, fluorescence hybridization. Proc Natl Acad Sci USA. 1986;83: 2934–2938. PubMed PMC

Zwick MS, Hanson RE, Islam-Faridi MN, Stelly DM, Wing RA, Price HJ, et al. A rapid procedure for the isolation of C 0 t-1 DNA from plants. Genome. 1997;40: 138–142. PubMed

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 Freitas NL, Al-Rikabi ABH, Bertollo LAC, Ezaz T, Yano CF, de Oliveira EA, et al. Early stages of XY sex chromosomes differentiation in the fish PubMed DOI PMC

de Moraes RLR, Bertollo LAC, Marinho MMF, Yano CF, Hatanaka T, Barby FF, et al. Evolutionary relationships and cytotaxonomy considerations in the genus PubMed DOI

de Oliveira EA, Sember A, Bertollo LAC, Yano CF, Ezaz T, Moreira-Filho O, et al. Tracking the evolutionary pathway of sex chromosomes among fishes: characterizing the unique XX/XY1Y2 system in PubMed DOI

Carvalho PC, de Oliveira EA, Bertollo LAC, Yano CF, Oliveira C, Decru E, et al. First chromosomal analysis in Hepsetidae (Actinopterygii, Characiformes): Insights into relationship between African and Neotropical fish groups. Front Genet. 2017; 8: 203 10.3389/fgene.2017.00203 PubMed DOI PMC

Hatanaka T, de Oliveira EA, Ráb P, Yano CF, Bertollo LAC, Ezaz T, et al. First chromosomal analysis in

Levan A, Fredga K, Sandberg AA. Nomenclature for centromeric position on chromosomes. Hereditas. 1964;52.

Sambrook J, Russell DW. Molecular Cloning, A Laboratory Manual New York: Cold Spring Harbor Laboratory Press; 2001.

Barby F, Rab P, Lavoue S, Ezaz T, Bertollo LAC, Kilian A, et al. From chromosomes to genome: insights into the evolutionary relationships and biogeography of Old World knifefishes (Notopteridae; Osteoglossiformes). Genes. 2018; 9: 306. PubMed PMC

Kilian A, Wenzl P, Huttner E, Carling J, Xia L, Blois H, et al. Diversity arrays technology: a generic genome profiling technology on open platforms In Data production and analysis in population genomics. Humana Press, Totowa, NJ; 2012. pp. 67–89. PubMed

Lambert MR, Skelly DK, Ezaz T. Sex-linked markers in the North American green frog ( PubMed DOI PMC

Dice LR. Measures of the amount of ecologic association between species. Ecology. 1945;26: 297–302.

Lê S, Josse J, Husson F. FactoMineR: an R package for multivariate analysis. J Stat Softw. 2008;25: 1–18.

Suzuki R, Shimodaira H. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics. 2006;22: 1540–1542. 10.1093/bioinformatics/btl117 PubMed DOI

Traut W, Winking H. Meiotic chromosomes and stages of sex chromosome evolution in fish: zebrafish, platyfish and guppy. Chromosom Res. 2001;9: 659–672. PubMed

Targino Valente G, Henrique Schneider C, Claudia Gross M, Feldberg E, Martins C. Comparative cytogenetics of cichlid fishes through genomic in-situ hybridization (GISH) with emphasis on Oreochromis niloticus. Chromosom Res. 2009; 17: 791–799. PubMed

Koubová M, Pokorná MJ, Rovatsos M, Farkačová K, Altmanová M, Kratochvíl L. Sex determination in Madagascar geckos of the genus PubMed

Altmanová M, Rovatsos M, Kratochvíl L, Johnson Pokorná M. Minute Y chromosomes and karyotype evolution in Madagascan iguanas (Squamata: Iguania: Opluridae). Biol J Linn Soc. 2016; 118: 618–633.

Trifonov VA, Vorobieva NN, Rens W. FISH with and without COT1 DNA Fluorescence In Situ Hybridization (FISH)—Application Guide. Springer; 2009. pp. 99–109.

Hilton EJ, Lavoué S. A review of the systematic biology of fossil and living bony-tongue fishes, Osteoglossomorpha (Actinopterygii: Teleostei). Neotrop Ichthyol. 2018;16: 1–35.

Urushido T. Karyotype of three species of fishes in the order Osteoglossiformes. Chromosom Inform Serv. 1975;18: 20–22.

Hirata J, Urushido T. Karyotypes and DNA content in the Osteoglossiformes. Sci Rep Res Inst Evol Biol. 2000;9: 83–90.

Ozouf-Costaz C, Coutanceau J-P, BOnillO C, Belkadi L, Fermon Y, Agnèse J-F, et al. First insights into karyotype evolution within the family Mormyridae. Cybium. 2015;39: 227–236.

Gornung E. Twenty years of physical mapping of major ribosomal RNA genes across the teleosts: a review of research. Cytogenet Genome Res. 2013;141: 90–102. 10.1159/000354832 PubMed DOI

Sochorová J, Garcia S, Gálvez F, Symonová R, Kovařík A. Evolutionary trends in animal ribosomal DNA loci: introduction to a new online database. Chromosoma. 2017; 1–10. 10.1007/s00412-016-0573-x PubMed DOI PMC

Majtánová Z, Symonová R, Arias‐Rodriguez L, Sallan L, Ráb P. “Holostei versus Halecostomi” problem: insight from cytogenetics of ancient Nonteleost Actinopterygian fish, bowfin PubMed

Symonová R, Majtánová Z, Arias‐Rodriguez L, Mořkovský L, Kořínková T, Cavin L, et al. Genome Compositional Organization in Gars Shows More Similarities to Mammals than to Other Ray‐Finned Fish. J Exp Zool Part B Mol Dev Evol. 2017;328: 607–619. PubMed

Milhomem SSR, Scacchetti PC, Pieczarka JC, Ferguson-Smith MA, Pansonato-Alves JC, O’Brien PCM, et al. Are NORs always located on homeologous chromosomes? A FISH investigation with rDNA and whole chromosome probes in PubMed DOI PMC

Sember A, Bohlen J, Šlechtová V, Altmanová M, Pelikánová Š, Ráb P. Dynamics of tandemly repeated DNA sequences during evolution of diploid and tetraploid botiid loaches (Teleostei: Cobitoidea: Botiidae). PLoS One. 2018;13: 1–27. PubMed PMC

Hillis DM, Dixon MT. Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol. 1991;66: 411–453. PubMed

Symonová R, Vrbová I, Lamatsch D, Paar J, Matzke-Karasz R, Schmit O, et al. Karyotype variability and inter-population genomic differences in freshwater ostracods (Crustacea) showing geographical parthenogenesis. Genes. 2018;9: 150. PubMed PMC

Vialle RA, de Souza JES, de Paiva Lopes K, Teixeira DG, de Azevedo Alves Sobrinho P, Ribeiro-dos-Santos AM, et al. Whole genome sequencing of the pirarucu (Arapaima gigas) supports independent emergence of major teleost clades. Genome Biol Evol. 2018;10: 2366–2379. 10.1093/gbe/evy130 PubMed DOI PMC

Bian C, Hu Y, Ravi V, Kuznetsova IS, Shen X, Mu X, et al. The Asian arowana ( PubMed DOI PMC

Delprat A, Negre B, Puig M, Ruiz A. The transposon PubMed PMC

Bailey JA, Baertsch R, Kent WJ, Haussler D, Eichler EE. Hotspots of mammalian chromosomal evolution. Genome Biol. 2004;5: R23 10.1186/gb-2004-5-4-r23 PubMed DOI PMC

Axelsson E, Webster MT, Smith NGC, Burt DW, Ellegren H. Comparison of the chicken and turkey genomes reveals a higher rate of nucleotide divergence on microchromosomes than macrochromosomes. Genome Res. 2005;15: 120–125. 10.1101/gr.3021305 PubMed DOI PMC

Webber C, Ponting CP. Hotspots of mutation and breakage in dog and human chromosomes. Genome Res. 2005;15: 1787–1797. 10.1101/gr.3896805 PubMed DOI PMC

Cavalli G, Misteli T. Functional implications of genome topology. Nat Struct Mol Biol. 2013;20: 290–299. 10.1038/nsmb.2474 PubMed DOI PMC

Fraser J, Williamson I, Bickmore WA, Dostie J. An overview of genome organization and how we got there: from FISH to Hi-C. Microbiol Mol Biol Rev. 2015;79: 347–372. 10.1128/MMBR.00006-15 PubMed DOI PMC

Razin SV, Gavrilov AA, Vassetzky YS, Ulianov SV. Topologically-associating domains: gene warehouses adapted to serve transcriptional regulation. Transcription. 2016;7: 84–90. 10.1080/21541264.2016.1181489 PubMed DOI PMC

Hrbek T, Farias IP, Crossa M, Sampaio I, Porto JIR, Meyer A. Population genetic analysis of

Araripe J, Rêgo PS do, Queiroz H, Sampaio I, Schneider H. Dispersal capacity and genetic structure of PubMed DOI PMC

Bertollo LAC, Moreira-Filho O, Galetti PM. Cytogenetics and taxonomy: consideration based on chromosome studies of freshwater fish. J Fish Biol. 1986;28.

de Oliveira EA, Bertollo LAC, Yano CF, Liehr T, Cioffi M de B. Comparative cytogenetics in the genus PubMed DOI PMC

Oliveira C, Toledo LFA, Foresti F, Toledo F SA. Supernumerary chromosomes, robertsonian rearrangement and multiple NORs in

Pellestor F, Anahory T, Lefort G, Puechberty J, Liehr T, Hédon B. Complex chromosomal rearrangements: origin and meiotic behavior. Hum Reprod Updat. 2011;17: 476–494. PubMed

Bird CE, Fernandez-Silva I, Skillings DJ, Toonen RJ. Sympatric speciation in the post “modern synthesis” era of evolutionary biology. Evol Biol. 2012;39: 158–180.

Smadja CM, Butlin RK. A framework for comparing processes of speciation in the presence of gene flow. Mol Ecol. 2011;20: 5123–5140. 10.1111/j.1365-294X.2011.05350.x PubMed DOI

Ortiz-Barrientos D, Engelstädter J, Rieseberg LH. Recombination rate evolution and the origin of species. Trends Ecol Evol. 2016;31: 226–236. 10.1016/j.tree.2015.12.016 PubMed DOI

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

Feldberg E, Porto JIR, Bertollo LAC. Chromosomal changes and adaptation of cichlid fishes during evolution In Val AL, Kapoor BG. Fish Adaptation. New Dehli: Science Publishers; 2003; pp. 285–308.

Hilton EJ. Comparative osteology and phylogenetic systematics of fossil and living bony-tongue fishes (Actinopterygii, Teleostei, Osteoglossomorpha). Zool J Linn Soc. 2003;137: 1–100.

Li G-Q, Wilson MVH, Grande L. Review of

Cytogenetics Meets Genomics: Cytotaxonomy and Genomic Relationships among Color Variants of the Asian Arowana Scleropages formosus

Comparison of Karyotypes in Two Hybridizing Passerine Species: Conserved Chromosomal Structure but Divergence in Centromeric Repeats

Present and Future Salmonid Cytogenetics