Skip to main content
SpringerLink
Log in

Comparative cytogenomic analysis of Cardinal fishes (Perciformes, Apogonidae) from Thailand

  • Original Article
  • Published:
The Nucleus Aims and scope Submit manuscript

Abstract

Cardinal fishes (Apogonidae) belong to the numerically dominating reef fish families. Many species are kept in the aquarium and are popular as small, peaceful, and colorful fish. The taxonomic status of this family remains debatable. Up to the present, there are 366 valid species. However, only 15 species were studied cytogenetically including one by molecular cytogenetics. Here we report characterization of four cardinal fishes, namely Fibramia lateralis, Pterapogon kauderni, Sphaeramia nematotera and S. orbicularis from the Gulf of Thailand using different cytogenomic approaches. Chromosome preparations from kidney were studied by conventional staining, Ag-NOR banding and molecular cytogenetics by fluorescence in situ hybridization (FISH) using 18S rDNA and microsatellite d(CA)15 probes. Whereas, all species had the same diploid chromosome number as 2n = 46, but there were differences in the fundamental number (NF) and chromosome structure: F. lateralis (NF = 54; 8a + 38t), S. nematotera (NF = 74; 14sm + 14a + 18t), S. orbicularis (NF = 68; 8sm + 14a + 24t) and P.kauderni (NF = 92; 4 m + 14sm + 28a). In all four species, NORs and 18S rDNA signals were detected adjacent to the telomere on the short arm of an acrocentric chromosome pair, but on different chromosome pairs, as 2, 10, 7 and 13 in F. lateralis, S. nematotera,S. orbicularis and P.kauderni, respectively. Also, microsatellite d(CA)15 sequences showed specific hybridization patterns along the chromosomes of the four studied species. Accordingly, all four Apogonidae species studied were clearly distinguishable by cytogenetic and molecular hybridization procedures. Further studies with more species are needed to explore their systematic status in the family

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Almeida-Toledo LF, Ozouf-Costaz C, Foresti F, Bonillo C, Porto-Foresti F, Daniel-Silva MFZ. Conservation of the 5S-bearing chromosome pair and co–localization with major rDNA clusters in five species of Astyanax (Pisces, Characidae). Cytogenet Genome Res. 2002;97:229–33. https://doi.org/10.1159/000066609.

    Article  CAS  PubMed  Google Scholar 

  2. Alvarez MC, Otis J, Amores A, Guise K. Short-term cell culture technique for obtaining chromosomes in marine and freshwater fish. J Fish Biol. 1991;39:817–24. https://doi.org/10.1111/j.1095-8649.1991.tb04411.x.

    Article  Google Scholar 

  3. Arai R. Fish karyotypes a check list. Tokyo: Springer Press; 2011.

    Book  Google Scholar 

  4. Araújo WC, Martínez PA, Molina WF. Mapping of ribosomal DNA by FISH, EcoRI digestion and replication bands in the cardinalfish Apogon americanus(Perciformes). Cytologia. 2010;75:109–17. https://doi.org/10.1508/cytologia.75.109.

    Article  Google Scholar 

  5. Chaiyasut K. Cytogenetics and Cytotaxonomy of the Family Zephyranthes. Department of Botany, Faculty of Science, Chulalongkorn University, Bangkok. 1989; [In Thai]

  6. Cioffi MB, Bertollo LAC. Distribution and evolution of repetitive DNAs in fish. Repetitive DNA Karger Genome Dyn Basel. 2012;7:197–221. https://doi.org/10.1159/000337950.

    Article  CAS  Google Scholar 

  7. Cioffi MB, Martins C, Bertollo LAC. Comparative chromosome mapping of repetitive sequences. Implications for genomic evolution in the fish. Hopliasmalabaricus BMCGenet. 2009;10:34. https://doi.org/10.1186/1471-2156-10-34.

    Article  CAS  Google Scholar 

  8. Cioffi MB, Bertollo Martins C, LAC. . Chromosomal spreading of associated transposable elements and ribosomal DNA in the fish Erythrinuserythrinus. Implications for genome change and karyoevolution in fish. BMC Evol Biol. 2010;10:271. https://doi.org/10.1186/1471-2148-10-271.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cioffi MB, Bertollo LAC, Villa MA, de Oliveira EA, Tanomtong A, Yano CF, Supiwong W, Chaveerach A. Genomic organization of repetitive DNA elements and its implications for the chromosomal evolution of Channid fishes (Actinopterygii, Perciformes). PLoS ONE. 2015;10(6):e0130199. https://doi.org/10.1371/journal.pone.0130199.

    Article  CAS  PubMed Central  Google Scholar 

  10. Cross I, Merlo A, Manchado M, Infante C, Cañavate JP. Rebordinos L. Cytogenetic characterization of the sole Solea senegalensis (Teleostei: Pleuronectiformes: Soleidae): Ag-NOR, (GATA)n, (TTAGGG)n and ribosomal genes by one-color and two-color FISH. Genetica. 2006;128:253–9. https://doi.org/10.1007/s10709-005-5928-9.

    Article  PubMed  Google Scholar 

  11. Eschmeyer WN, Fong JD. Species by family/subfamily. On-line Updated 30 April 2018, ]Accessed 23 May 2018] http://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp.

  12. Eschmeyer WN, Fricke R, Laan R. van der (eds). Catalog of fishes: Genera, Species, References. On-line Updated 2 July 2018 [Accessed 3 July 2018]http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp.

  13. Fontana F, Lanfredi M, Congiu L, Leis M, Chicca M, Rossi R. Chromosomal mapping of 18S–28S and 5S rRNA genes by two-colour fluorescent in situ hybridization in six sturgeon species. Genome. 2003;46:473–7. https://doi.org/10.1139/g03-007.

    Article  CAS  PubMed  Google Scholar 

  14. Getlekha N, Cioffi MB, Maneechot N, Bertollo LAC, Supiwong W, Tanomtong A. Contrasting evolutionary paths among Indo-Pacific Pomacentrus species promoted by extensive pericentric inversions and genome organization of repetitive sequences. Zebrafish. 2018;15(1):45–54. https://doi.org/10.1089/zeb.2017.1484.

    Article  CAS  PubMed  Google Scholar 

  15. Getlekha N, Cioffi MB, Yano CF, Maneechot N, Bertollo LAC, Supiwong W, et al. Chromosome mapping of repetitive DNAs in sergeant major fishes (Abudefdufinae, Pomacentridae): a general view on the chromosomal conservatism of the genus. Genetica. 2016;144(5):567–76. https://doi.org/10.1007/s10709-016-9925-y.

    Article  CAS  PubMed  Google Scholar 

  16. Getlekha N, Molina WF, Cioffi MB, Yano CF, Maneechot N, Bertollo LAC, Supiwong W, Tanomtong A. Repetitive DNAs highlight the role of chromosomal fusions in the karyotype evolution of Dascyllus species (Pomacentridae, Perciformes). Genetica. 2016;144(2):203–11. https://doi.org/10.1007/s10709-016-9890-5.

    Article  PubMed  Google Scholar 

  17. Hatanaka T, Galetti PM Jr. Mapping of the 18S and 5S ribosomal RNA genes in the fish Prochilodus argenteus Agassiz, 1829 (Characiformes, Prochilodontidae). Genetica. 2004;122:239–44. https://doi.org/10.1007/s10709-004-2039-y.

    Article  CAS  PubMed  Google Scholar 

  18. Howell WM, Black DA. Controlled silver–staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia. 1980;36:1014–5. https://doi.org/10.1007/BF01953855.

    Article  CAS  PubMed  Google Scholar 

  19. Hsu TC, Patak S, Chen TR. The possibility of latent centromeres and a proposed nomenclature system for total chromosome and whole arm translocations. Cytogenet Cell Genet. 1975;15:41–9. https://doi.org/10.1159/000130497.

    Article  CAS  PubMed  Google Scholar 

  20. Johnson GD, Gill AC, Paxton JR, Eschmeyer WN, editors. Encyclopedia of Fishes. San Diego: Academic Press; 1998.

    Google Scholar 

  21. Kasiroek W, Indananda C, Luangoon N, Pinthong K, Supiwong W, Tanomtong A. First chromosome analysis of the Humpback cardinalfish, Fibramia lateralis (Perciformes, Apogonidae). Cytologia. 2017;82(1):9–15. https://doi.org/10.1508/cytologia.82.9.

    Article  Google Scholar 

  22. Kasiroek W, Indananda C, Pinthong K, Supiwong W, Tanomtong A. NOR polymorphism and chromosome analysis of Banggai cardinalfish, Pterapogonkauderni (Perciformes, Apogonidae). Cytologia. 2017;82(1):17–23. https://doi.org/10.1508/cytologia.82.17.

    Article  Google Scholar 

  23. Kubat Z, Hobza R, Vyskot B, Kejnovsky E. Microsatellite accumulation in the Y chromosome of Silene latifolia. Genome. 2008;51:350–6. https://doi.org/10.1139/G08-024.

    Article  CAS  PubMed  Google Scholar 

  24. Mabuchi K, Fraser TH, Song H, Azuma Y, Nishida M. Revision of the systematics of the cardinalfishes (Percomorpha: Apogonidae) based on molecular analyses and comparative reevaluation of morphological characters. Zootaxa. 2014;3846(2):151–203. https://doi.org/10.11646/zootaxa.3846.2.1.

    Article  PubMed  Google Scholar 

  25. Maneechot N, Yano CF, Bertollo LAC, Getlekha N, Molina WF, Ditcharoen S, et al. Genomic organization of repetitive DNAs highlights chromosomal evolution in the genus Clarias (Clariidae, Siluriformes). Mol Cytogenet. 2016;9:4. https://doi.org/10.1186/s13039-016-0215-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Murofushi M. A study of karyotype classification and karyotype evolution in marine teleosts. Rep Mishima Res Inst Sci Liv Nihon Univ . 1986;9:95–157.

    Google Scholar 

  27. Murofushi M, Oishi M, Nawa N. Karyological studies in Apogonsemilineatus. Rep Mishima Res Inst Sci Liv Nihon Univ. 1980;3:47–50.

    Google Scholar 

  28. Nelson JS. Fishes of the World. 4th ed. New York: John Wiley & Sons; 2006.

    Google Scholar 

  29. Ojima Y, Kojima T. Chromosomal polymorphisms in Apogonidae fishes. Proc Jpn Acad Ser B Phys Biol Sci. 1985;61:79–82.

    Article  Google Scholar 

  30. Pinkel D, Straume T, Gray J. Cytogenetic analysis using quantitative, high sensitivity, fluorescence hybridization. In: Proceedings of the National Academy of Sciences of the United States of America.1986; 83: 29–34.

  31. Rishi KK. A preliminary report on the karyotypes of eighteen marine fishes. Res Bull Punjab Univ. 1973;24:161–2.

    Google Scholar 

  32. Rivlin KA, Dale G, Rachlin JW. Karyotypic analysis of three species of cardinalfish (Apogonidae)and its implications for the taxonomic status of the genera Apogon and Phaeoptyx. Ann N Y Acad Sci. 1986;463:211–3. https://doi.org/10.1111/j.1749-6632.1986.tb21549.x.

    Article  Google Scholar 

  33. Rivlin KA, Rachlin JW, Dale G. Intraspecific chromosomal variation in Apogonbinotatus(Perciformes: Apogonidae)from the Florida Keys and St.Croix.Ann. N. Y. Acad Sci. 1987;494:263–5. https://doi.org/10.1111/j.1749-6632.1987.tb29542.x.

    Article  Google Scholar 

  34. Rivlin KA, Rachlin JW, Warkentine BE. G-Banding of the chromosomes of Apogonmaculates and A. pseudomaculatus (Perciformes:Apogonidae). Ann N Y Acad Sci. 1988;529:160–3. https://doi.org/10.1111/j.1749-6632.1988.tb51448.x.

    Article  Google Scholar 

  35. Rooney DE. Human cytogenetics: constutitional analysis: a practical approach. 3rd ed. London: Oxford University Press; 2001.

    Google Scholar 

  36. Rosa R, Bellafronte E, Moreira-Filho O, Margarido VP. Constitutive heterochromatin, 5S and 18S rDNA genes in Apareiodon sp. (Characiformes, Parodontidae) with a ZZ/ZW sex chromosome system. Genetica. 2006;128:159–66. https://doi.org/10.1007/s10709-005-5700-1.

    Article  CAS  PubMed  Google Scholar 

  37. Schmidt M. Chromosome banding in Amphibia. II. Constitutive heterochromatin and nucleolus organizer regions in Ranidae, Microhylidae and Racophoridae. Chromosoma. 1978;68:131–48.

    Article  Google Scholar 

  38. Supiwong W, Jiwyam W, Sreeputhorn K, Maneechot N, Bertollo LAC, Cioffi MB, Getlekha N, et al. First reports on classical and molecular cytogenetics of archerfish, Toxoteschatareus(Perciformes: Toxotidae). Nucleus (India). 2017;60(3):349–59. https://doi.org/10.1007/s13237-017-0216-5.

    Article  Google Scholar 

  39. Supiwong W, LiehrT Cioffi MB, Chaveerach A, KosyakovaN Fan X, Tanee T, Tanomtong A. Comparative cytogenetic mapping of rRNA genes among naked catfishes: implications for genomic evolution in the Bagridae family. Genet Mol Res. 2014;13(4):9533–42. https://doi.org/10.4238/2014.November.12.2.

    Article  CAS  PubMed  Google Scholar 

  40. Supiwong W, LiehrT Cioffi MB, Chaveerach A, KosyakovaN Pinthong K, Tanee T, Tanomtong A. Chromosomal evolution in naked catfishes (Bagridae, Siluriformes): a comparative chromosome mapping study. Zool Anz. 2014;253:316–20. https://doi.org/10.1016/j.jcz.2014.02.004.

    Article  Google Scholar 

  41. Suzuki H, Kurihara Y, Kanemisha Y, Moriwaki K. Variation in the distribution of silver-staining nucleolar organizer regions on the chromosomes of the wild mouseMus musculus. Mol Biol Evol. 1990;7:271–82. https://doi.org/10.1093/oxfordjournals.molbev.a040598.

    Article  CAS  PubMed  Google Scholar 

  42. Turpin R, Lejeune J. Les chromosomes humains. Paris: Gauthier-Pillars; 1965.

    Google Scholar 

  43. Volff NJ. Sex determination in fish. Genome Biol. 2002. https://doi.org/10.1186/gb-2002-3-9-reports0052.

    Article  Google Scholar 

  44. Wasko AP, Galetti PM Jr. Mapping 18S ribosomal genes in fish of the genus Brycon (Characidae) by fluorescence in situ hybridization (FISH). Genet Mol Biol. 2000;23(1):135–8. https://doi.org/10.1590/S1415-47572000000100025.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Research grant of Burapha University through National Research Council of Thailand (Grant No. 158/2560), Unit of Excellence 2021 on Genetic diversity assessment of widely distributed aquatic animals and herpetology from Thailand (UoE64003).

Author information

Authors and Affiliations

  1. Institute of Marine Science, Burapha University, Muang, 20131, Chonburi, Thailand

    Wannapa Kasiroek

  2. Biology Program, Faculty of Science and Technology, Phetchabun Rajabhat University, Phetchabun, 67000, Thailand

    Sumalee Phimphan & Surachest Aiumsumang

  3. Department of Fundamental Science, Faculty of Science and Technology, SurindraRajabhat University, Muang, 32000, Surin, Thailand

    Krit Pinthong

  4. Department of Fishery, School of Agriculture and Natural Resources, University of Phayao, Muang, 56000, Phayao, Thailand

    Chatmongkon Suwannapoom

  5. Institute of Human Genetics, Jena University Hospital, Friedrich Schiller University, Am Klinikum 1, 07747, Jena, Germany

    Thomas Liehr

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

    Weerayuth Supiwong

  7. Department of Biology, Faculty of Science, KhonKaen University, Muang, 40002, KhonKaen, Thailand

    Alongklod Tanomtong

Authors
  1. Wannapa Kasiroek
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sumalee Phimphan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Krit Pinthong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chatmongkon Suwannapoom
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Surachest Aiumsumang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Thomas Liehr
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Weerayuth Supiwong
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alongklod Tanomtong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Weerayuth Supiwong.

Ethics declarations

Conflict of interest

The author declares that they have no conflict of interest.

Ethics approval

The Animal Ethics Committee of Burapha University based on the Ethic of Animal Experimentation of National Research Council of Thailand, ID#19/ 2558.

Consent to participate

Yes.

Consent for publication

Yes.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Corresponding Editor: RN Chatterjee

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kasiroek, W., Phimphan, S., Pinthong, K. et al. Comparative cytogenomic analysis of Cardinal fishes (Perciformes, Apogonidae) from Thailand. Nucleus 65, 57–66 (2022). https://doi.org/10.1007/s13237-021-00352-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13237-021-00352-5

Keywords

Search

Navigation