Korean Journal of Ecology and Environment (생태와환경)

The Korean Society of Limnology (한국수생태학회)
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Occurrence of a Natural Interspecific Hybrid between Rhodeus pseudosericeus and R. notatus in Sangcheon Stream of the Han River, Korea

한강수계 상천천에서 한강납줄개 Rhodeus pseudosericeus와 떡납줄갱이 R. notatus의 종간 자연잡종 출현

  • Kwak, Yeong-Ho (Inland Fisheries Research Institute, National Institute of Fisheries Science) ;
  • Kim, Keun-Yong (AquaGenTech Co., Ltd) ;
  • Kim, Keun-Sik (Research Center for Endangered species, National Institute of Ecology) ;
  • Song, Ha-Yun (Inland Fisheries Research Institute, National Institute of Fisheries Science)
  • 곽영호 (국립수산과학원 중앙내수면연구소) ;
  • 김근용 (아쿠아진텍) ;
  • 김근식 (국립생태원 멸종위기종복원센터) ;
  • 송하윤 (국립수산과학원 중앙내수면연구소)
  • Received : 2020.08.31
  • Accepted : 2020.09.23
  • Published : 2020.09.30
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Abstract

Two specimens presumed to be hybrids of Rhodeus pseudosericeus and R. notatus were collected from the Sangcheon Stream of the Han River, Korea. The body color of natural hybrid individuals was yellowish brown, showing the intermediate characteristics of R. pseudosericeus and R. notatus, but overall, the characteristics of R. notatus were similar. Meristic and morphometric characters, the number of dorsal fin rays, anal fin rays and longitudinal row scales showed a hybrid index (HI) of 0, indicating the characters of R. notatus. The hybrid index of predorsal length (HI=74.6), preanal length (HI=75.3), and preventral length (HI=77.6) were similar to the characters of the R. pseudosericeus. Also four characters were appeared to have intermediate characters between R. pseudosericeus and R. notatus; number of gill rakers (HI=55.3), body depth (HI=67.9), snout length (HI=43.4), and inter orbital width (HI=44.8). The rest of 14 characters deviated between 0 and 100, showing unique characteristics of hybrid individuals. Recombination activating gene 1 (RAG1) analysis, hybrids were identified as natural hybrids due to the overlapping peaks of their parent species. Also, as a result of analysis using the cytochrome b gene (COB), one individual was derived from R. pseudosericeus, while the other was derived from R. notatus.

한강수계 상천천에서 한강납줄개 Rhodeus pseudosericeus와 떡납줄갱이 R. notatus의 잡종으로 추정되는 2개체를 채집하였다. 자연잡종 개체의 체색은 황갈색으로 한강납줄개와 떡납줄갱이의 중간적인 특성을 나타냈지만, 전반적으로 떡납줄갱이의 특징이 두드러졌다. 계수 및 계측형질에서 등지느러미 기조수, 뒷지느러미 기조수, 종렬비늘 수의 3가지 형질은 hybrid index (HI) 값이 0으로 나타나 떡납줄갱이의 형질을 따랐다. 체장에 대한 등지느러미 기점 거리 (HI=74.6), 뒷지느러미 기점 거리 (HI=75.3), 배지느러미 기점 거리 (HI =77.6)는 한강납줄개의 형질을 따르는 것으로 나타났다. 새파수(HI=55.3), 체장에 대한 체고(HI=67.9), 두장에 대한 문장(HI=43.4), 양안간격(HI=44.8)의 4가지 형질은 한강납줄개와 떡납줄갱이의 중간형질을 나타내는 것으로 나타났다. 나머지 14가지 형질은 0과 100 사이를 벗어나 잡종개체만의 고유한 특성을 나타냈다. Recombination activating gene 1 (RAG1) 분석결과 잡종개체는 부모종의 유전자가 중복되어 나타나 자연잡종으로 판별되었으며, cytochrome b gene (COB)를 분석한 결과 한 개체는 한강납줄개를 모계로, 또 다른 한 개체는 떡납줄갱이가 모계로 나타났다.

Keywords

References

  1. Abbott, R., D. Albach, S. Ansell, J.W. Arntzen, S.J.E. Baird, N. Bierne, J. Boughman, A. Brelsford, C.A. Buerkle, R. Buggs, R.K. Butlin, U. Dieckmann, F. Eroukhmanoff, A. Grill, S.H. Cahan, J.S. Hermansen, G. Hewitt, A.G. Hudson, C. jiggins, J. Jones, B. Keller, T. Marczewski, J. Mallet, P. Martinez-Rodriguez, M. Most, S. Mullen, R. Nichols, A.W. Nolte, C. Parisod, K. Pfennig, A.M. Rice, M.G. Ritchie, B. Seifert, C.M. Smadja, R. Stelkens, J.M. Szymura, R. Vainola, J.B.W. Wolf and D. Zinner. 2013. Hybridization and speciation. Journal of Evolutionary Biology 26: 229-246. https://doi.org/10.1111/j.1420-9101.2012.02599.x
  2. Avise, J.C. and N.C. Saunders. 1984. Hybridization and introgression among species of sunfish (Lepomis): analysis by mitochondrial DNA and allozyme markers. Genetics 108: 237-255. https://doi.org/10.1093/genetics/108.1.237
  3. Begg, G.A. and J.R. Waldman. 1999. An holistic approach to fish stock identification. Fisheries Research 43: 35-44. https://doi.org/10.1016/S0165-7836(99)00065-X
  4. Billington, N. and P.D. Hebert. 1991. Mitochondrial DNA diversity in fishes and its implications for introductions. Canadian Journal of Fisheries and Aquatic Sciences 48: 80-94. https://doi.org/10.1139/f91-306
  5. Chae, B.S., H.B. Song and J.Y. Park. 2019. A field guide to the freshwater fishes of Korea. LG evergreen foundation, Seoul, Korea.
  6. Cebrat, M., A. Cebula, A. Laszkiewicz, M. Kasztura, A. Miazek and P. Kisielow. 2008. Mechanism of lymphocyte-specific inactivation of RAG-2 intragenic promoter of NWC: implications for epigenetic control of RAG locus. Molecular Immunology 45: 2297-2306. https://doi.org/10.1016/j.molimm.2007.11.009
  7. Demarais, B.D., T.E. Dowling, M.E. Douglas, W.L. Minckley and P.C. Marsh. 1992. Origin of Gila seminuda (Teleostei: Cyprinidae) through introgressive hybridization: implications for evolution and conservation. Proceedings of the National Academy of Sciences 89: 2747-2751. https://doi.org/10.1073/pnas.89.7.2747
  8. Economidis, P.S. and A.I. Sinis. 1988. A natural hybrid of Leuciscus cephalus macedonicus${\times}$Chalcalburnus chalcoides macedonicus (Pisces, Cyprinidae) from Lake Volvi (Macedonia, Greece). Journal of Fish Biology 32: 593-605. https://doi.org/10.1111/j.1095-8649.1988.tb05398.x
  9. Eyualem, A. and M. Blaxter. 2003. Comparison of biological, molecular, and morphological methods of species identification in a set of cultured Panagrolaimus isolates. Journal of Nematology 35: 119-128.
  10. Hubbs, C.L. 1955. Hybridization between fish species in nature. Systematic Zoology 4: 1-20. https://doi.org/10.2307/2411933
  11. Hubbs, C.L. and K.F. Lagler. 2004. Fishes of the Great Lakes region, revised edition, revised edition. The Unversity of Michigan Press, USA.
  12. Jansson, H., I. Holmgren, K. Wedin and T. Andersson. 1991. High frequency of natural hybrids between Atlantic salmon, Salmo salar L., and brown trout, S. trutta L., in a Swedish river. Journal of Fish Biology 39: 343-348. https://doi.org/10.1111/j.1095-8649.1991.tb05096.x
  13. Jerry, D.R., T.A. Raadik, S.C. Cairns and P.R. Baverstock. 1999. Evidence for natural interspecific hybridization between the Australian bass (Macquaria novemaculeata) and estuary perch (M. colonorum). Marine and Freshwater Research 50: 661-666. https://doi.org/10.1071/MF98120
  14. Kang, E.J., C.H. Kim, I.S. Park, H. Yang and Y.C. Cho. 2006. Early developmental characteristics of induced hybrids between Rhodeus uyekii and R. notatus (Pisces: Cyprinidae). Korean Journal of Ichthyology 18: 339-346.
  15. Kerschbaumer, M., L. Postl, M. Koch, T. Wiedl and C. Sturmbauer. 2011. Morphological distinctness despite largescale phenotypic plasticity-analysis of wild and pond-bred juveniles of allopatric populations of Tropheus moorii. Naturwissenschaften 98: 125-134. https://doi.org/10.1007/s00114-010-0751-2
  16. Kim, B.S., E.J. Kang, H. Jang and I.S. Park. 2012. Morphometric traits and cytogenetic analysis in induced cross and reciprocal hybrid between Rhodeus uyekii and R. notatus. Korean Journal of Ichthyology 24: 151-159.
  17. Kim, C.H., E.J. Kang and J.H. Kim, 2006. Development of eggs and early life history of Korean bitterling, Rhodeus pseudosericeus (Acheilognathinae). Korean Journal of Ichthyology 18: 266-272.
  18. Kim, C.H., W.O. Lee, Y.J. Kang and J.M. Baek. 2010. Occurrence of a natural intergeneric hybrid, Rhodeus uyekii${\times}$Acheilognathus signifer (Pisces; Cyprinidae) from Jojongcheon Bukhan River, Korea. Korean Journal of Ichthyology 22: 225-229.
  19. Kim, H.S. and J.Y. Park. 2020. Spawning characteristics of Hangang bitterling, Rhodeus pseudosericeus (Pisces: Acheilognathinae) in the host mussel with Glochidia. Korean Journal of Ichthyology 32: 63-69. https://doi.org/10.35399/ISK.32.2.4
  20. Kim, H.S., J.D. Yoon, H. Yang, H.S. Choi and J.H. Lee. 2017. Reproductive characteristics of Rhodeus pseudosericeus (Pisces: Acheilognathinae) in the Heukcheon, Namhangang (River), Korea. Korean Journal of Ichthyology 29: 235-243.
  21. Kim, H.S., S.W. Yun, H.T. Kim and J.Y. Park. 2015b. Occurrence of a natural hybrid between Acheilognathus signifer and A. lanceolatus (Pisces: Cyprinidae). Korean Journal of Ichthyology 27: 199-204.
  22. Kim, H.S., S.W. Yun, J.G. Ko and J.Y. Park. 2014. Occurrence of a natural intergeneric hybrid between Rhodeus pseudosericeus and Acheilognathus signifer (Pisces: Cyprinidae) from the Namhangang (river), Korea. Korean Journal of Ichthyology 26: 153-158.
  23. Kim, I.S. and J.Y. Park. 2002. Freshwater Fishes of Korea. Kyohak Publishing, Seoul, Korea.
  24. Kim, I.S., Y. Choi, C.L. Lee, Y.J. Lee, B.J. Kim and J.H. Kim. 2005. Illustrated book of Korean fishes. Kyohak publishing, Seoul, Korea.
  25. Kim, K.Y. and I.C. Bang. 2010. Molecular phylogenetic position of Abbottina springeri (Cypriniformes: Cyprinidae) based on nucleotide sequences of RAG1 gene. Korean Journal of Ichthyology 22: 273-278.
  26. Kim, K.Y., M.H. Ko, S.J. Cho, W.J. Kim, M.H. Son and I.C. Bang. 2015a. A natural hybrid of intergeneric mating between a female Pungtungia herzi and a male Pseudorasbora parva (Cypriniformes: Cyprinidae). Fisheries and Aquatic Sciences 18: 99-107. https://doi.org/10.5657/FAS.2015.0099
  27. Kim, P., J.H. Han and S.L. An. 2020. Genetic identification of species and natural hybridization determination based on mitochondrial DNA and nuclear DNA of genus Zacco in Korea. Mitochondrial DNA Part A 31: 221-227. https://doi.org/10.1080/24701394.2020.1777994
  28. Ko, M.H., M.S. Han and S.M. Kwan. 2018. Distribution aspect and extinction threat evaluation of the endangered species, Rhodeus pseudosericeus (Pisces: Cyprinidae) in Korea. Korean Journal of Ichthyology 30: 100-106. https://doi.org/10.35399/ISK.30.2.5
  29. Ko, M.H., R.Y. Myung and H.S. Kim, 2019. Fish community characteristics and habitat aspects of endangered species, Rhodeus pseudosericeus in Heuk Stream, a tributary of the Han River drainage system. Korean Journal of Environment and Ecology 33: 266-279. https://doi.org/10.13047/KJEE.2019.33.3.266
  30. Kucinski, M., K. Demska-Zakes, D. Zarski, T. Liszewski, D. Fopp-Bayat, M. Jankun and G. Furgala-Selezniow. 2015. The morphological, histological and cytogenetic characteristics of goldfish Carassius auratus (L.)${\times}$common carp Cyprinus carpio (L.) hybrids. Caryologia 68: 77-83. https://doi.org/10.1080/00087114.2015.1021154
  31. Larsson Herrera, S., C. Tha, R.R. Vetukuri, A. Knight, L.J. Grenville-Briggs and M. Tasin. 2020. Monitoring and discrimination of Pandemis moths in apple orchards using semiochemicals, wing pattern morphology and DNA barcoding. Crop Protection 132: 105-110.
  32. Lee, I.R., H. Yang, J.H. Kim, K.Y. Kim and I.C. Bang. 2009. Identification of a natural hybrid between the striped spine loach Cobitis tetralineata and the king spine loach Iksookimia longicorpa by analyzing mitochondrial COI and nuclear RAG1 sequences. Korean Journal of Ichthyology 21: 287-290.
  33. Lee, S.H. 2013. Impacts of weirs on fish community in the Jojong Stream. Master Dissertation, Seoul National University.
  34. McDonald, J.H., R. Seed and R.K. Koehn. 1991. Allozymes and morphometric characters of three species of Mytilus in the Northern and Southern Hemispheres. Marine Biology 111: 323-333. https://doi.org/10.1007/BF01319403
  35. ME (Ministry of Environment). 2005. Enforcement of Wildlife Laws (Law No. 7167).
  36. ME (Ministry of Environment). 2012. Conservation and Management Laws of wildlife (Law No. 10977).
  37. MOCT (Ministry of Construction Transportation). 1989. River improvement master plan of Jojong Stream. Gyeonggi Province.
  38. MOCT (Ministry of Construction Transportation). 2003. River improvement master plan of Jojong Stream. Gyeonggi Province.
  39. Nam, M.M. 1997. The fish fauna and community structure in the Jojong Stream. Korean Journal of Limnology 30: 367-376.
  40. Nelson, J.S., T.C. Grande and M.V.H. Wilson. 2016. Fishs of the World (Fifth edition). John Wiley & Sons, Hoboken, New Jersey, USA.
  41. Nguyen, K.B., J. Maruniak and B.J. Adams, 2001. Diagnostic and phylogenetic utility of the rDNA internal transcribed spacer sequences of Steinernema. Journal of Nematology 33: 73-82.
  42. NIBR (National Institute of Biological Resources). 2019. Red data book of republic of Korea (second edition), volume 3 (Freshwater fishes). Ministry of Environment, Incheon, Korea.
  43. Nikoljukin, M.J. 1972. Distant hybridization in Acipenseridae and Teleostei, theory and practice, Moscow.
  44. Ramoejane, M., G. Gouws, E.R. Swartz, B.L. Sidlauskas and O.L. Weyl. 2020. Molecular and morphological evidence reveals hybridisation between two endemic cyprinid fishes. Journal of Fish Biology 96: 1234-1250. https://doi.org/10.1111/jfb.14153
  45. Ross, M.R. and T.M. Cavender. 1981. Morphological analyses of four experimental intergeneric cyprinid hybrid crosses. Copeia 2: 377-387. https://doi.org/10.2307/1444226
  46. Scribner, K.T., K.S. Page and M.L. Bartron. 2001. Hybridization in freshwater fishes: a review of case studies and cytonuclear methods of biological inference. Reviews in Fish Biology and Fisheries 10: 293-323. https://doi.org/10.1023/A:1016642723238
  47. Slechtova, V., J. Bohlen and H.H. Tan. 2007. Families of Cobitoidea (Teleostei; Cypriniformes) as revealed from nuclear genetic data and the position of the mysterious genera Barbucca, Psilorhynchus, Serpenticobitis and Vaillantella. Molecular Phylogenetics and Evolution 44: 1358-1365. https://doi.org/10.1016/j.ympev.2007.02.019
  48. Song, H.Y., J.H. Kim, I.Y. Seo and I.C. Bang. 2017. Species and hybrid identification of Genus Coreoleuciscus species in Hwnag-ji Stream, Nakdong River basin in Korea. Korean Journal of Ichthyology 29: 1-12.
  49. Sonnenberg, R., A. Nolte and D. Tautz. 2007. An evaluation of LSU rDNA D1-D2 sequences for their use in species identification. Frontiers in Zoology 4: 1-12. https://doi.org/10.1186/1742-9994-4-1
  50. Soric, V.M. 2004. A natural hybrid of Leuciscus cephalus and Alburnus alburnus (Pisces, Cyprinidae) from the Ibar River, Western Serbia. Archives of Biological Sciences 56: 23-32. https://doi.org/10.2298/ABS0402023S
  51. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690. https://doi.org/10.1093/bioinformatics/btl446
  52. Stamatakis, A., P. Hoover and J. Rougemont. 2008. A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57: 758-771. https://doi.org/10.1080/10635150802429642
  53. Tang, Q.Y., S.Q. Liu, D. Yu, H.Z. Liu and P.D. Danley. 2012. Mitochondrial capture and incomplete lineage sorting in the diversification of balitorine loaches (Cypriniformes, Balitoridae) revealed by mitochondrial and nuclear genes. Zoologica Scripta 41: 233-247. https://doi.org/10.1111/j.1463-6409.2011.00530.x
  54. Verspoor, E. and J. Hammart. 1991. Introgressive hybridization in fishes: the biochemical evidence. Journal of Fish Biology 39: 309-334. https://doi.org/10.1111/j.1095-8649.1991.tb05094.x
  55. Vitule, J.R.S., C.A. Freire and D. Simberloff. 2009. Introduction of non-native freshwater fish can certainly be bad. Fish and Fisheries 10: 98-108. https://doi.org/10.1111/j.1467-2979.2008.00312.x
  56. Wirtz, P. 1999. Mother species?father species: unidirectional hybridization in animals with female choice. Animal Behaviour 58: 1-12. https://doi.org/10.1006/anbe.1999.1144
  57. Witkowski, A., J. Kotusz, K. Wawer, J. Stefaniak, M. Popiolek and J. Blachuta. 2015. A natural hybrid of Leuciscus leuciscus (L.) and Alburnus alburnus (L.) (Osteichthyes: Cyprinidae) from the Bystrzyca River (Poland). Annales Zoologici 65: 287-293. https://doi.org/10.3161/00034541ANZ2015.65.2.010
  58. Yi, S., J. Zhong, S. Huang, S. Wang and W. Wang. 2017. Morphological comparison and DNA barcoding of four closely related species in the genera Misgurnus and Paramisgurnus (Cypriniformes: Cobitidae). Biochemical Systematics and Ecology 70: 50-59. https://doi.org/10.1016/j.bse.2016.10.019
  59. Yun, Y.E., I.R. Lee, S.Y. Park, E.J. Kang, E.O. Kim, S.K. Yang, Y.K. Nam and I.C. Bang. 2009. Genetic Identification of Hybrids between Rhodeus uyekii and R. notatus by Sequence Analysis of RAG-1 Gene. Journal of Aquaculture 22: 79-82.