Notopteridae (Teleostei, Osteoglossiformes) represents an old fish lineage with ten currently recognized species distributed in African and Southeastern Asian rivers. Their karyotype structures and diploid numbers remained conserved over long evolutionary periods, since African and Asian lineages diverged approximately 120 Mya. However, a significant genetic diversity was already identified for these species using molecular data. Thus, why the evolutionary relationships within Notopteridae are so diverse at the genomic level but so conserved in terms of their karyotypes? In an attempt to develop a more comprehensive picture of the karyotype and genome evolution in Notopteridae, we performed comparative genomic hybridization (CGH) and cross-species (Zoo-FISH) whole chromosome painting experiments to explore chromosome-scale intergenomic divergence among seven notopterid species, collected in different African and Southeast Asian river basins. CGH demonstrated an advanced stage of sequence divergence among the species and Zoo-FISH experiments showed diffuse and limited homology on inter-generic level, showing a temporal reduction of evolutionarily conserved syntenic regions. The sharing of a conserved chromosomal region revealed by Zoo-FISH in these species provides perspectives that several other homologous syntenic regions have remained conserved among their genomes despite long temporal isolation. In summary, Notopteridae is an interesting model for tracking the chromosome evolution as it is (i) ancestral vertebrate group with Gondwanan distribution and (ii) an example of animal group exhibiting karyotype stasis. The present study brings new insights into degree of genome divergence vs. conservation at chromosomal and sub-chromosomal level in representative sampling of this group.

Departamento de Biologia Estrutural Molecular e Genética Universidade Estadual de Ponta Grossa Ponta Grossa PR 84030 900 Brazil

Departamento de Genética e Evolução Universidade Federal de São Carlos Rodovia Washington Luiz Km 235 C P 676 São Carlos SP 13565 905 Brazil

Department of Cellular Biology and Genetics Biosciences Center Federal University of Rio Grande do Norte Natal Brazil

Department of Fisheries and Aquaculture Adamawa State University P M B 25 Mubi Adamawa State Nigeria

Institute for Applied Ecology University of Canberra Canberra ACT 2617 Australia

Institute of Human Genetics University Hospital Jena 07747 Jena Germany

Laboratório de Cultura de Tecidos e Citogenética SAMAM Instituto Evandro Chagas Belém Brazil

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

Molecular and Cellular Biology Russian Academy of Sciences Novosibirsk Russia

Toxic Substances in Livestock and Aquatic Animals Research Group KhonKaen University Muang KhonKaen 40002 Thailand

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Bănărescu, P. Zoogeography of Fresh Waters. General Distribution and Dispersal of FreshwaterAnimals (Aula-Verlag, 1990).

Greenwood, P. H., Wilson, M. V., Paxton, J. R. & Eschmeyer, W. N. Encyclopedia of Fishes (Academic Press: San Diego, 1998).

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. doi: 10.1046/j.1096-3642.2003.00032.x. DOI

Sallan LC. Major issues in the origins of ray‐finned fish (Actinopterygii) biodiversity. Biol. Rev. 2014;89:950–971. doi: 10.1111/brv.12086. PubMed DOI

Darlington, P. J. Zoogeography (John Wiley: New York, 1957).

Hilton, E. J. & Lavoué, S. A review of the systematic biology of fossil and living bony-tongue fishes, Osteoglossomorpha (Actinopterygii: Teleostei). Neotrop. Ichthyol.16, e180031 (2018).

Nelson, J. S., Grande, T. C. & Wilson, M. V. H. Fishes of the World (John Wiley & Sons, Hoboken, 2016).

Austin CM, Tan MH, Croft LJ, Hammer MP, Gan HM. Whole genome sequencing of the Asian arowana (Scleropages formosus) provides insights into the evolution of ray-finned fishes. Genome Biol. Evol. 2015;7:2885–2895. doi: 10.1093/gbe/evv186. PubMed DOI PMC

Barby, F. et al. From chromosomes to genome: insights into the evolutionary relationships and biogeography of Old World knifefishes (Notopteridae; Osteoglossiformes). Genes, 10.3390/genes9060306 (2018). PubMed PMC

Bian C, et al. The Asian arowana (Scleropages formosus) genome provides new insights into the evolution of an early lineage of teleosts. Sci. Rep. 2016;6:1–17. doi: 10.1038/s41598-016-0001-8. PubMed DOI PMC

Canitz J, Kirschbaum F, Tiedemann R. Karyotype description of the African weakly electric fish Campylomormyrus compressirostris in the context of chromosome evolution in Osteoglossiformes. J. Physiol. Paris. 2016;110:273–280. doi: 10.1016/j.jphysparis.2017.01.002. PubMed DOI

Ozouf-Costaz C, et al. First insights into karyotype evolution within the family Mormyridae. Cybium. 2015;39:227–236.

Ráb P, et al. Karyotype and mapping of repetitive DNAs in the african butterfly fish Pantodon buchholzi, the sole species of the family Pantodontidae. Cytogenet. Genome Res. 2016;149:312–320. doi: 10.1159/000450534. PubMed DOI

Eschmeyer, W. N. & Fong, J. Species by family/subfamily in the Catalog of fishes, electronic version (07 November 2018). San Francisco (California Academy of Sciences) (2018).

Roberts TR. Systematic revision of the old world freshwater fish family Notopteridae. Ichthyol. Explor. Freshw. 1992;2:361–383.

Vidthayanon, C. Thailand red data: fishes (Office of Natural Resources and Environmental Policy and Planning Bangkok, Thailand, 2005).

Inoue JG, Kumazawa Y, Miya M, Nishida M. The historical biogeography of the freshwater knifefishes using mitogenomic approaches: a Mesozoic origin of the Asian notopterids (Actinopterygii: Osteoglossomorpha) Mol. Phylogenet. Evol. 2009;51:486–499. doi: 10.1016/j.ympev.2009.01.020. PubMed DOI

Ráb, P., Rábová, M., Pereira, C. S., Collares-Pereira, M. J. & Pelikánová, S. Chromosome studies of European cyprinid fishes: interspecific homology of leuciscine cytotaxonomic marker–the largest subtelocentric chromosome pair as revealed by cross-species painting. Chromosome Res16, (2008). PubMed

Nagamachi, C. Y. et al. Multiple rearrangements in cryptic species of electric knifefish, Gymnotus carapo (Gymnotidae, Gymnotiformes) revealed by chromosome painting. BMC Genet. 11, 28 (2010). PubMed PMC

Symonová, R. et al. Genome differentiation in a species pair of coregonine fishes: an extremely rapid speciation driven by stress - activated retrotransposons mediating extensive ribosomal DNA multiplications. BMC Evol Biol. 13, (2013). PubMed PMC

Yano CF, et al. Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae) Heredity (Edinb). 2017;118:276–283. doi: 10.1038/hdy.2016.83. PubMed DOI PMC

de Freitas NL, et al. Early Stages of XY sex chromosomes differentiation in the fish Hoplias malabaricus (Characiformes, Erythrinidae) revealed by DNA repeats accumulation. Curr. Genomics. 2018;19:216–226. doi: 10.2174/1389202918666170711160528. PubMed DOI PMC

de Moraes RLR, et al. Evolutionary relationships and cytotaxonomy considerations in the genus Pyrrhulina (Characiformes, Lebiasinidae) Zebrafish. 2017;14:536–546. doi: 10.1089/zeb.2017.1465. PubMed DOI

Sember A, et al. Sex chromosome evolution and genomic divergence in the fish Hoplias malabaricus (Characiformes, Erythrinidae) Front. Genet. 2018;9:71. doi: 10.3389/fgene.2018.00071. PubMed DOI PMC

Traut W, Winking H. Meiotic chromosomes and stages of sex chromosome evolution in fish: zebrafish, platyfish and guppy. Chromosome Res. 2001;9:659–672. doi: 10.1023/A:1012956324417. PubMed DOI

Schemberger MO, et al. Differentiation of repetitive DNA sites and sex chromosome systems reveal closely related group in Parodontidae (Actinopterygii: Characiformes) Genetica. 2011;139:1499–1508. doi: 10.1007/s10709-012-9649-6. PubMed DOI

Vicari MR, et al. New insights on the origin of B chromosomes in Astyanax scabripinnis obtained by chromosome painting and FISH. Genetica. 2011;139:1073–1081. doi: 10.1007/s10709-011-9611-z. PubMed DOI

Scudeler PES, Diniz D, Wasko AP, Oliveira C, Foresti F. Whole chromosome painting of B chromosomes of the red-eye tetra Moenkhausia sanctaefilomenae (Teleostei, Characidae) Comp. Cytogenet. 2015;9:661–669. doi: 10.3897/CompCytogen.v9i4.5460. PubMed DOI PMC

Utsunomia R, et al. Uncovering the ancestry of B chromosomes in Moenkhausia sanctaefilomenae (Teleostei, Characidae) PLoS One. 2016;11:e0150573. doi: 10.1371/journal.pone.0150573. PubMed DOI PMC

Knytl M, Kalous L, Symonová R, Rylková K, Ráb P. Chromosome studies of European cyprinid fishes: cross-species painting reveals natural allotetraploid origin of a Carassius female with 206 chromosomes. Cytogenet. Genome Res. 2013;139:276–283. doi: 10.1159/000350689. PubMed DOI

Fujiwara A, Abe S, Yamaha E, Yamazaki F, Yoshida MC. Uniparental chromosome elimination in the early embryogenesis of the inviable salmonid hybrids between masu salmon female and rainbow trout male. Chromosoma. 1997;106:44–52. doi: 10.1007/s004120050223. PubMed DOI

Sakai C, et al. Chromosome elimination in the interspecific hybrid medaka between Oryzias latipes and O. hubbsi. Chromosome Res. 2007;15:697–709. doi: 10.1007/s10577-007-1155-9. PubMed DOI

Poltronieri J, et al. Comparative chromosomal mapping of microsatellites in Leporinus species (Characiformes, Anostomidae): unequal accumulation on the W chromosomes. Cytogenet. Genome Res. 2014;142:40–5. doi: 10.1159/000355908. PubMed DOI

Molina WF, et al. Preferential accumulation of sex and Bs chromosomes in biarmed karyotypes by meiotic drive and rates of chromosomal changes in fishes. An. Acad. Bras. Cienc. 2014;86:1801–1812. doi: 10.1590/0001-3765201420130489. PubMed DOI

Getlekha N, et al. Contrasting evolutionary paths among indo-pacific Pomacentrus species promoted by extensive pericentric inversions and genome organization of repetitive sequences. Zebrafish. 2018;15:45–54. doi: 10.1089/zeb.2017.1484. PubMed DOI

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. doi: 10.1016/j.ympev.2016.03.008. PubMed DOI

White, M. J. D. Modes of speciation. (San Francisco: WH Freeman 455p.-Illus., maps, chrom. nos General (KR, 197800185), 1978).

King, M. Species evolution: the role of chromosome change (Cambridge University Press, 1995).

Coyne, J. A. & Orr, H. A. Speciation. Sinauer Associates, Inc.: Sunderland, 2004).

Potter S, et al. Chromosomal speciation in the genomics era: disentangling phylogenetic evolution of rock-wallabies. Front. Genet. 2017;8:10. doi: 10.3389/fgene.2017.00010. PubMed DOI PMC

Molina WF, Martinez PA, Bertollo LAC, Bidau CJ. Evidence for meiotic drive as an explanation for karyotype changes in fishes. Mar. Genomics. 2014;15:29–34. doi: 10.1016/j.margen.2014.05.001. PubMed DOI

Mank JE, Avise JC. Phylogenetic conservation of chromosome numbers in Actinopterygiian fishes. Genetica. 2006;127:321–327. doi: 10.1007/s10709-005-5248-0. PubMed DOI

Brum MJ, Galetti PM., Jr. Teleostei ground plan karyotype. J. Comp. Biol. 1997;2:91–102.

Motta Neto CC, Lima-Filho PA, Araújo WC, Bertollo LAC, Molina WF. Differentiated evolutionary pathways in Haemulidae (Perciformes): karyotype stasis versus morphological differentiation. Rev. Fish Biol. Fish. 2012;22:457–465. doi: 10.1007/s11160-011-9236-4. DOI

Neto CCM, Cioffi MB, Bertollo LAC, Molina WF. Extensive chromosomal homologies and evidence of karyotypic stasis in Atlantic grunts of the genus Haemulon (Perciformes) J. Exp. Mar. Bio. Ecol. 2011;401:75–79. doi: 10.1016/j.jembe.2011.02.044. DOI

Mazzuchelli J, Kocher TD, Yang F, Martins C. Integrating cytogenetics and genomics in comparative evolutionary studies of cichlid fish. BMC Genomics. 2012;13:463. doi: 10.1186/1471-2164-13-463. PubMed DOI PMC

Molina, W. F. Chromosomal changes and stasis in marine fish groups. Fish Cytogenet. 69–110 (2007).

Brum MJI. Cytogenetic studies of Brazilian marine fish. Braz. J. Genet. 1996;19:421–427.

Soares, R. X. et al. Chromosomal evolution in large pelagic oceanic apex predators, the barracudas (Sphyraenidae, Percomorpha). Genet. Mol. Res. Genet. Mol. Res16, (2017). PubMed

Molina WF, Galetti PM., Jr. Karyotypic changes associated to the dispersive potential on Pomacentridae (Pisces, Perciformes) J. Exp. Mar. Bio. Ecol. 2004;309:109–119. doi: 10.1016/j.jembe.2004.03.011. DOI

Ellegren H. Evolutionary stasis: the stable chromosomes of birds. Trends Ecol. Evol. 2010;25:283–291. doi: 10.1016/j.tree.2009.12.004. PubMed DOI

Farré M, Robinson TJ, Ruiz‐Herrera A. An integrative breakage model of genome architecture, reshuffling and evolution. Bioessays. 2015;37:479–488. doi: 10.1002/bies.201400174. PubMed DOI

Costa GWWF, Cioffi MB, Bertollo LAC, Molina WF. Structurally complex organization of repetitive DNAs in the genome of Cobia (Rachycentron canadum) Zebrafish. 2015;12:215–220. doi: 10.1089/zeb.2014.1077. PubMed DOI

Cordaux R, Batzer MA. The impact of retrotransposons on human genome evolution. Nat. Rev. Genet. 2009;10:691. doi: 10.1038/nrg2640. PubMed DOI PMC

Bailey, J. A., Baertsch, R., Kent, W. J., Haussler, D. & Eichler, E. E. Hotspots of mammalian chromosomal evolution. Genome Biol.5, (2004). PubMed PMC

Peng JC, Karpen GH. Epigenetic regulation of heterochromatic DNA stability. Curr. Opin. Genet. Dev. 2008;18:204–211. doi: 10.1016/j.gde.2008.01.021. PubMed DOI PMC

Sotero-Caio CG, Platt RN, Suh A, Ray DA. Evolution and diversity of transposable elements in vertebrate genomes. Genome Biol. Evol. 2017;9:161–177. doi: 10.1093/gbe/evw264. PubMed DOI PMC

Feliciello I, Chinali G, Ugarković Đ. Structure and population dynamics of the major satellite DNA in the red flour beetle Tribolium castaneum. Genetica. 2011;139:999. doi: 10.1007/s10709-011-9601-1. PubMed DOI

Kantek DLZ, et al. Chromosomal location and distribution of As51 satellite DNA in five species of the genus Astyanax (Teleostei, Characidae, Incertae sedis) J. Fish Biol. 2009;75:408–421. doi: 10.1111/j.1095-8649.2009.02333.x. PubMed DOI

Nanda I, Karl E, Griffin DK, Schartl M, Schmid M. Chromosome repatterning in three representative parrots (Psittaciformes) inferred from comparative chromosome painting. Cytogenet. Genome Res. 2007;117:43–53. doi: 10.1159/000103164. PubMed DOI

de Oliveira EHC, et al. Chromosome reshuffling in birds of prey: the karyotype of the world’s largest eagle (Harpy eagle, Harpia harpyja) compared to that of the chicken (Gallus gallus) Chromosoma. 2005;114:338–343. doi: 10.1007/s00412-005-0009-5. PubMed DOI

Tagliarini MM, O’Brien P, Ferguson-Smith MA, de Oliveira EHC. Maintenance of syntenic groups between Cathartidae and Gallus gallus indicates symplesiomorphic karyotypes in new world vultures. Genet. Mol. Biol. 2011;34:80–83. doi: 10.1590/S1415-47572010005000117. PubMed DOI PMC

Pokorná, M. et al. Strong conservation of the bird Z chromosome in reptilian genomes is revealed by comparative painting despite 275 million years divergence. Chromosoma120, (2011). PubMed

Balmus G, et al. Cross-species chromosome painting among camel, cattle, pig and human: further insights into the putative Cetartiodactyla ancestral karyotype. Chromosome Res. 2007;15:499. doi: 10.1007/s10577-007-1154-x. PubMed DOI

Kulemzina AI, et al. Chromosome painting in Tragulidae facilitates the reconstruction of Ruminantia ancestral karyotype. Chromosome Res. 2011;19:531. doi: 10.1007/s10577-011-9201-z. PubMed DOI

Valente GT, Schneider CH, Gross MC, Feldberg E, Martins C. Comparative cytogenetics of cichlid fishes through genomic in-situ hybridization (GISH) with emphasis on Oreochromis niloticus. Chromosome Res. 2009;17:791. doi: 10.1007/s10577-009-9067-5. PubMed DOI

Lim KY, et al. Sequence of events leading to near‐complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol. 2007;175:756–763. doi: 10.1111/j.1469-8137.2007.02121.x. PubMed DOI

Majka J, Majka M, Kwiatek M, Wiśniewska H. Similarities and differences in the nuclear genome organization within Pooideae species revealed by comparative genomic in situ hybridization (GISH) J. Appl. Genet. 2017;58:151–161. doi: 10.1007/s13353-016-0369-y. PubMed DOI PMC

Matsuoka MP, Gharrett AJ, Wilmot RL, Smoker WW. Genetic linkage mapping of allozyme loci in even-and odd-year pink salmon (Oncorhynchus gorbuscha) J. Hered. 2004;95:421–429. doi: 10.1093/jhered/esh069. PubMed DOI

Machado MdA, et al. Extensive karyotype reorganization in the fish Gymnotus arapaima (Gymnotiformes, Gymnotidae) highlighted by Zoo-FISH analysis. Front. Genet. 2018;9:8. doi: 10.3389/fgene.2018.00008. PubMed DOI PMC

Backström N, et al. Genetic mapping in a natural population of collared flycatchers (Ficedula albicollis): conserved synteny but gene order rearrangements on the avian Z chromosome. Genetics. 2006;174:377–386. doi: 10.1534/genetics.106.058917. PubMed DOI PMC

Skinner BM, Griffin DK. Intrachromosomal rearrangements in avian genome evolution: evidence for regions prone to breakpoints. Heredity. 2012;108:37–41. doi: 10.1038/hdy.2011.99. PubMed DOI PMC

Bertollo, L. A. C., Cioffi, M. B. & Moreira-Filho, O. Direct chromosome preparation from Freshwater Teleost Fishes BT - Fish cytogenetic techniques (Chondrichthyans and Teleosts). In (eds Ozouf-Costaz, C., Pisano, E., Foresti, F. & Almeida Toledo, L. F.) (Enfield USA, 10.1201/b18534-4 (2015).

Yang, F., Trifonov, V., Ng, B. L., Kosyakova, N. & Carter, N. P. Generation of paint probes by flow-sorted and microdissected chromosomes BT - Fluorescence In Situ Hybridization (FISH)–Application Guide. In (ed. Liehr, T.), 10.1007/978-3-540-70581-9_3 (2009).

Zwick MS, et al. A rapid procedure for the isolation of C0t-1 DNA from plants. Genome. 1997;40:138–142. doi: 10.1139/g97-020. PubMed DOI

Sambrook, J. & Russell, D. W. Molecular Cloning, A Laboratory Manual (Cold Spring Harbor Laboratory Press, 2001).

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. 118–131 (2015).

Levan, A., Fredga, K. & Sandberg, A. A. Suggestion for a chromosome nomenclature based on centromeric position. Hereditas52, (1964).

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Cross-Species BAC Mapping Highlights Conservation of Chromosome Synteny across Dragon Lizards (Squamata: Agamidae)

Taxonomic Diversity Not Associated with Gross Karyotype Differentiation: The Case of Bighead Carps, Genus Hypophthalmichthys (Teleostei, Cypriniformes, Xenocyprididae)

Centric Fusions behind the Karyotype Evolution of Neotropical Nannostomus Pencilfishes (Characiforme, Lebiasinidae): First Insights from a Molecular Cytogenetic Perspective

Interspecific Genetic Differences and Historical Demography in South American Arowanas (Osteoglossiformes, Osteoglossidae, Osteoglossum)

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Karyotypes and Sex Chromosomes in Two Australian Native Freshwater Fishes, Golden Perch (Macquaria ambigua) and Murray Cod (Maccullochella peelii) (Percichthyidae)

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