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Morphologies and population genetic structures of the eight-barbel loach of the genus Lefua on southern Sakhalin

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Abstract

Coldwater, primary freshwater, fish such as the eight-barbel loach, Lefua nikkonis, are thought to have colonised Hokkaido from the continental Far East via Sakhalin Island during the Late Pleistocene. Lefua populations have been reported on southern Sakhalin, but detailed morphological and population structure analyses have not yet been completed. This information is important for reconstructing the colonisation history of L. nikkonis to Hokkaido. In this study, morphological analysis revealed that L. nikkonis and two continental congeners, Lefua pleskei and Lefua costata, are distinguishable from each other, and Lefua collected from southern Sakhalin is morphologically more similar to L. nikkonis. Random forest analysis, a machine learning classification method, classified all Sakhalin individuals as L. nikkonis. Haplotype analysis of mitochondrial DNA sequences revealed that all but one Sakhalin haplotype are shared with L. nikkonis and none is shared with the two continental congeners, which supports the hypothesis that Sakhalin Lefua are L. nikkonis. However, none of the Sakhalin haplotypes was distributed on northern Hokkaido. This discontinuous distribution of haplotypes across Sakhalin and Hokkaido suggests that the Sakhalin Lefua populations are not native. Some of the Sakhalin haplotypes were found only on Hokkaido’s Ishikari River system or the Tokachi River system, suggesting that they originated from these regions. Because previous field surveys reported wild Lefua only from northwestern Sakhalin, we concluded that native Lefua on southern Sakhalin may have gone extinct after they colonised Hokkaido in the Middle Pleistocene.

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References

  • Avise JC (2000) Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge

    Google Scholar 

  • Bogutskaya NG, Naseka AM (1996) Cyclostomata and fishes of Khanka Lake drainage area (Amur river basin): an annotated check-list with comments on taxonomy and zoogeography of the region. Zoological Institute of Russian Academy of Sciences, St. petersburg

  • Bogutskaya NG, Naseka AM, Shedko SV, Vasil’eva ED, Chereshnev IA (2008) The fishes of the Amur River: updated check-list and zoogeography. Ichthyol Explor Freshw 19: 301–366

    Google Scholar 

  • Breiman L (2001) Random Forests. Mach Learn 45: 5–32

    Article  Google Scholar 

  • Cutler DR, Edwards Jr. TC, Beard KH, Cutler A, Hess KT, Gibson J, Lawler JJ (2007) Random forests for classification in ecology. Ecology 88: 2783–2792

    Article  Google Scholar 

  • Díaz-Uriarte, De Andrés SA (2006) Gene selection and classification of microarray data using random foreset. BMC bioinformatics 7: 3

    Article  Google Scholar 

  • Dyldin YV, Orlov AM (2016) Ichthyofauna of Fresh and Brackish Waters of Sakhalin Island: An Annotated List with Taxonomic Comments: 2. Cyprinidae–Salmonidae Families. J Ichthyol 56: 656–693

    Article  Google Scholar 

  • Goto A, Nakano S (1993) Distribution and ecology of freshwater fishes in Hokkaido. In: Higashi S, Osawa A, Kanagawa K (eds) Biodiversity and Ecology in the Northernmost Japan. Hokkaido University Press, Sapporo, pp 113–126

    Google Scholar 

  • Higuchi H (2012) Bird migration and the conservation of the global environment. J Ornithol 153: 3–14

    Article  Google Scholar 

  • Hirsch PE, Guyen AN, Muller R, Adrian-Kalchhauser I, Burkhardt-Holm P (2018) Colonizing Islands of water on dry land - on the passive dispersal of fish eggs by birds. Fish Fish 19: 1–9

    Article  Google Scholar 

  • Hosoya K (2013) Cobitidae loaches. In: Nakabo T (ed) Fishes of Japan with pictorial keys to the species third edition. Tokai University Press, Kanagawa, pp 333 and 1821

  • Karafutoteichi Gyogyousuisan Kumiai (Sakhalin Fixed Fishery Association) (1931) Karafuto to gyogyou (Sakhalin and Fishery). Kogyokan Printing Co., Hokkaido

    Google Scholar 

  • Karafutocho (Sakhalin Prefecture) (1973) Karafutochoshisei sanjyunenshi (jyou) [Sakhalin Prefecture: A administrative history of the first 30 years (the first part)]. Harashobou, Tokyo

    Google Scholar 

  • Koizumi E, Usio N, Kawai T, Azuma N, Masuda R (2012) Loss of Genetic Diversity Means Loss of Geological Information: The Endangered Japanese Crayfish Exhibits Remarkable Historical Footprints. PLoS ONE 7: e33986

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  • Kuwahara T (2015) Lefua nikkonis (Jordan & Fowler, 1903). In: Ministry of the environment (ed) Red data book 2014. – threatened wildlife of Japan- volume 4, Pisces –brackish and fresh water fishes. Gyosei, Tokyo, pp 194–195

  • Labai, VS, Atamanova IA, Zavarzin DS, Motylkova IV, Moukhametova ON, Nikitin VD (2014) Reservoirs of the Sakhalin Island: from Lagoons to Lakes. Yuzhno-Sakhalinsk, Sakhalin

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  Google Scholar 

  • Lindberg GU (1972) Large-scale fluctuations of sea level in the Quaternary period: Hypothesis based on biogeographical evidence. Shinbori T, Kanemitsu F (transl.) (1981) Tokai Univ Press, Tokyo

  • Ministry of the environment (2019) Migratory bird related information. https://www.env.go.jp/nature/dobutsu/bird_flu/migratory/index.html. Accessed 17 August 2019

  • Nakajima J, Uchiyama R (2017) Loaches of Japan -natural history and culture. Yama-kei Publishers, Tokyo

    Google Scholar 

  • Naseka AM, Bogutskaya NG (2004) Contribution to taxonomy and nomenclature of freshwater fishes of the Amur drainage area and the Far East (Pisces, Osteichthyes). Zoosyst Ross 12: 279–290

    Google Scholar 

  • Nikoforov SN, Makeev SS, Belovolvo VF (1994) The freshwater ichthyofauna of southern Sakhalin and its origin. J Ichthyol 34: 24–41

    Google Scholar 

  • Novikov NP, Sokolovsky AS, Sokolovskaya TG, Yakovlev YM (2002) The fishes of Primorye. Far Eastern State Technical Fisheries Univ Press, Vladivostok

    Google Scholar 

  • Ooyagi A (2013) Distribution in the Shimokita Peninsula, Aomori Prefecture of Japanese Ezohotoke Lefua nikkonis (Cobitidae) and morphologic comparison with species of the Hokkaido Prefecture product. J Nat Hist Aomori 18:61–67

    Google Scholar 

  • Ooyagi A, Mokodongan DF, Montenegro J, Mandagi IF, Koizumi N, Machida Y, Inomata N, Shedko SV, Hutama AA, Hadiaty RK, Yamahira K (2018) Phylogeography of the eight-barbel loach Lefua nikkonis (Cypriniformes: Nemacheilidae): how important were straits in northern Japan as biogeographical barriers? Ichthyol Res 65:115–126

    Article  Google Scholar 

  • Pietsch TW, Bogatov VV, Storozhenko SY, Lelej AS, Barkalov VY, Takahashi H, Joneson SL, Kholin SK, Glew KA, Harpel JA, Krestov PV, Makarchenko EA, Minakawa N, Ôhara M, Bennett DJ, Anderson TR, Crawford RL, Prozorova LA, Kuwahara Y, Shedko SV, Yabe M, Woods PJ, Stevenson DE (2012) Biodiversity and biogeography of Sakhalin Island, in Flora and Fauna of North-West Pacific Islands (Materials of International Kuril Island and International Sakhalin Island Projects). Vladivostok Dal’nauka: 11–79

  • Safronov SN, Nikiforov SN (2003) The list of piciformes and fishes of the fresh and brackish water of Sakhalin. J Ichthyol 43: 38–49

    Google Scholar 

  • Sakai H, Ueda T, Yokoyama R, Safronov SN, Goto A (2014) Genetic structure and phylogeography of northern Far Eastern pond minnows, Rhynchocypris perenurus sachalinensis and R. p. mantschuricus (Pisces, Cyprinidae), inferred from mitochondrial DNA sequences. Biogeography 16: 87–109

    Google Scholar 

  • Shedko SV, Shedko MB (2003) New data on freshwater ichthyofauna of the south far east of Russia. Chteniya pamyati Vladimira Yakovlevicha Levanidova (Readings in Memoriam of Vladimir Yakovlevich Levanidov). Dalnauka 2: 319–336

    Google Scholar 

  • Shedko SV, Miroshnichenko IL, Nemkova GA (2008) On the systematics and phylogeography of eight-barbel loaches of the genus Lefua (Cobitoidea: Nemacheilidae): MtDNA typing of L. pleskei, Russ J Genet 44: 817–825

    Article  CAS  Google Scholar 

  • Shimizu M (2011) Seed production of endangered and threatened cypriniforms in Hokkaido, Japan. Master Theses, Faculty of Bioindustry, Tokyo University of Agriculture

    Google Scholar 

  • Soto CG, Burhanuddin, (1995) Clove oil as a fish anaesthetic for measuring length and weight of rabbitfish (Siganus lineatus). Aquaculture 136: 149–152

    Article  Google Scholar 

  • Sawada Y (2005) Lefua nikkonis. In: Kawanabe H, Mizuno N and Hosoya K (eds) Freshwater fishes of Japan. Yama-kei publishers, Tokyo, pp 401

    Google Scholar 

  • Takeuchi M, Ohta T (1993) Distribution and a few ecological aspects of Lefua costata nikkonis (Cobitididae) in Aomori Prefecture, Japan. Bull Biogeogr Soc Japan. 48:73–80

    Google Scholar 

  • Watanabe K, Takahashi H, Kitamura A, Yokoyama R, Kitagawa T, Takeshima H, Sato S, Yamamoto S, Takehana Y, Mukai T, Ohara K, Iguchi K (2006) Biogeographical history of Japanese freshwater fishes: Phylogeographic approaches and perspectives. Japan J Ichthyol 53: 1–38

    Google Scholar 

  • Zenkoku Karafuto Renmei (Japanese Sakhalin Federation) (1978) Karafutoenkaku gyouseishi (A History of Sakhalin Government). Matsui Pi Te O Printing, Tokyo

Download references

Acknowledgments

We express our gratitude to T. Kanno, H. Senou, Y. Uni, S. Yamada, K. Ushiyama, T. Kitano, A. Goto and T. Kuwahara for their valuable suggestions and F. Bastide for the English check. We are also grateful to S. Makeyev, K. Kimira and K. Amano for help in the field work. We are grateful to the following persons for giving us permission to examine specimens from their institutions: M. Miya and T. Sado (CBM), F. Tashiro (HUMZ) and K. Hagiwara (YCM). This work was partly supported by grants-in-aid to Y. Machida for the Akiyama life science foundation, Japan.

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Machida, Y., Kanaiwa, M., Shedko, S.V. et al. Morphologies and population genetic structures of the eight-barbel loach of the genus Lefua on southern Sakhalin. Ichthyol Res 68, 239–248 (2021). https://doi.org/10.1007/s10228-020-00783-1

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