Ichthyological Research

, Volume 66, Issue 1, pp 67–78 | Cite as

Trace of outbreeding between Biwa salmon (Oncorhynchus masou subsp.) and amago (O. m. ishikawae) detected from the upper reaches of inlet streams within Lake Biwa water system, Japan

  • Masayuki KuwaharaEmail author
  • Hiroshi Takahashi
  • Takeshi Kikko
  • Seiji Kurumi
  • Kei’ichiro Iguchi
Full Paper


The establishment of fluvial fish populations from anadromous populations by natural or artificial barriers obstructing migration is a good research subject to study life history plasticity. Biwa salmon, Oncorhynchus masou subsp., a salmonid fish endemic to the Lake Biwa water system, exhibit life history variation (e.g., mature stream-resident males) in addition to a typical lacustrine life history type, indicating potential adaptations of life histories in response to emergence of barriers. Currently, fluvial populations that are morphologically similar to both stream-resident Biwa salmon and amago, the fluvial red-spotted masu salmon, Oncorhynchus masou ishikawae, are found upstream of dams which were constructed in the inflowing rivers of Lake Biwa. However, it is unknown whether they are Biwa salmon or amago. To explore that, the genetic characteristics of nine fluvial populations were investigated through AFLP and mtDNA analyses. Bayesian admixture analysis based on the AFLP data revealed that three fluvial populations were admixed populations between Biwa salmon and amago. In addition, a Biwa salmon mtDNA haplotype was detected in some individuals from three populations. However, no genetically pure fluvial populations of Biwa salmon were found, indicating no life history plasticity in this subspecies, and thus hybridization with amago boosted the ability of this subspecies to establish fluvial populations. Nevertheless, other scenarios, such as hybridization after establishment of fluvial populations of Biwa salmon, are also possible. The latter hypothesis could be supported by the fact that amago did not inhabit the river before emergence of barriers. However, a significant genetic population structure was found only in amago, suggesting that this subspecies is native to the Lake Biwa water system. But the possibility that multiple sources of amago have been released into rivers cannot be excluded. Therefore, further studies on the relationships between amago populations in the upper reaches of the Lake Biwa water system and other populations in the surrounding areas of the Lake Biwa water system are needed to clarify the origins of the admixed populations.


Lake Biwa water system Oncorhynchus masou Crossbreeding mtDNA AFLP 



We thank Drs. Katsuro Yahiro, Yasufumi Satoguchi, Robin J. Smith, Ryoichi Tabata (Lake Biwa Museum), Prof. Kouichi Kawamura (Faculty of Bioresources, Mie University), and Dr. Kentaro Morita (Hokkaido National Fisheries Research Institute) for encouragement and critical reading of this manuscript. Our special thanks go to Mr. Makoto Kobayashi (Residing in Takashima), Mr. Noriyuki Ikeda (Chief of the Echi River upstream fishery cooperative), and Mr. Hayato Nishimura (Residing in Otsu) for valuable information on stocking Biwa salmon and amago, and upstream migrating Biwa salmon, respectively. We are also grateful to Mr. Akihiko Mori and members of his fishing group for sampling fish for this study. This work was conducted as part of a Collaborative Research Project of the Lake Biwa Museum (Kyo 06-02).

Supplementary material

10228_2018_650_MOESM1_ESM.xls (37 kb)
Supplementary material 1 (XLS 37 kb)
10228_2018_650_MOESM2_ESM.xls (128 kb)
Supplementary material 2 (XLS 128 kb)


  1. Anderson, EC (2008) Bayesian inference of species hybrids using multilocus dominant genetic markers. Phil Trans R Soc B 363:2841–2850Google Scholar
  2. Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229Google Scholar
  3. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE : a simulation study. Mol Ecol 14:2611–2620Google Scholar
  4. Excoffier L, Lischer H (2010) Arlequin suite ver. 3.5: a new series of programs to perform population genetics analysis under Linux and Windows. Mol Ecol Res 10:564–567Google Scholar
  5. Falush D, Stephens M, Pritchard JK. 2007. Structure software, Version 2.2. University of Oxford, OxfordGoogle Scholar
  6. Fujioka Y (1990) Biwa salmon : its ecological and morphological characteristics. Technical Reports of Hokkaido Salmon Hatchery (Fish and Eggs) 159:25–38Google Scholar
  7. Fujioka Y (1991) Morphological, physiological and ecological studies on Biwa salmon. BULL SHIGA PREF SAMEGAI TROU FARM 3:1–112Google Scholar
  8. Fujioka Y (2009) Introduction of Biwa salmon Migrating between River and Lake. Sunrise Shuppann, Hikone, 216ppGoogle Scholar
  9. Fujioka Y, Fushiki S (1988) Downstream migration and body silvering in underyearling Biwa salmon Oncorhynchus rhodurus. Nippon Suisan Gakkaishi 54:1889–1897Google Scholar
  10. Furukawa T (1989) Biwamasu: Oncorhynchus masou subsp. In:Kawanabe K, Mizuno N (eds) Freshwater fishes of Japan. Yamakei, Tokyo, pp 180–181Google Scholar
  11. Hosoya K (2013) 96. Family Salmonidae. In: Nakabo K (ed) Fishes of Japan with pictorial keys to the species third edition. Tokaidaigaku Shuppannkai, Kanagawa, pp 1833–1835Google Scholar
  12. Honjoh T (1977) Studies on culture and transplantation of Amago salmon salmon, Oncorhynchus rhodurus. Report of Gifu Prefectural Fresh Water Fish Research Institute 22:1–103Google Scholar
  13. Ichimura M, Yanagimoto T, Kobayashi T, Masaoka T, Kaeriyama M (2011) Hybrid identification of “Sakemasu” collected in the Nemuro Strait, eastern Hokkaido, using DNA analysis. Nippon Suisan Gakkaishi 77:834–844Google Scholar
  14. Kaeriyama M (1996) Effect of population density and habitat environment on life history strategy and migration of juvenile Sockeye (Oncorhynchus nerka) and Chum Salmon (O. keta). Scientific Reports of the Hokkaido Salmon Hatchery 50:101–111Google Scholar
  15. Kamata T (1979) The native stocks and transplantation of Amago salmon and Iwana trout in Shiga Prefecture. In: Shiga Shizen Kankyo Kenkyukai (ed) Land and life in Shiga: scientific studies of Shiga Prefecture, Japan. Foundation of Nature Conservation in Shiga Prefecture, Otsu, pp 615–622Google Scholar
  16. Kato F (1978) Morphological and ecological studies on two forms of Oncorhynchus rhodurus found in Lake Biwa and adjoining inlets. Jpn J Ichthyol 25:197–204Google Scholar
  17. Kato F (1981) The Amago salmon salmon, Oncorhynchus rhodurus, collected in Lake Biwa. Jpn J Ichthyol 28:184–186Google Scholar
  18. Kato K (1977) Natural hybrids of salmonid fishes from the Nippara River, Tokyo. Jpn J Ichthyol 23:225–232Google Scholar
  19. Kawabata J (1931) Fishes from Lake Biwa. The society that posthumaous published the late Mr. Jugorou Kawabata’s manuscript, Tokyo, 198ppGoogle Scholar
  20. Kikko T, Kuwahara M, Iguchi K, Kurumi S, Yamamoto S, Kai Y, Nakayama K (2008) Mitochondrial DNA Population Structure of the White-Spotted Charr (Salvelinus leucomaenis) in the Lake Biwa Water System. Zool Sci 25:146–153Google Scholar
  21. Kitano S, Hasegawa K, Maekawa K (2009) Evidence for interspecific hybridization between native white-spotted charr Salvelinus leucomaenis and non-native brown trout Salmo trutta on Hokkaido Island, Japan. J Fish Biol 74: 467–473Google Scholar
  22. Kitano S, Ohdachi S, Koizumi I, Hasegawa K (2014) Hybridization between native white-spotted charr and nonnative brook trout in the upper Sorachi River, Hokkaido, Japan. Ichthyol Res 61:1–8Google Scholar
  23. Kuwahara M (2013) Present status and conservation of the endemic subspecies of Oncorhynchus masou (Biwa salmon) in Lake Biwa. Jpn J Ichthyol 60:63–67Google Scholar
  24. Kuwahara M, Iguchi K (1994) Occurrence of mature stream resident males of Biwa salmon, Oncorhynchus masou subsp. Jpn J Ichthyol 40:495–497Google Scholar
  25. Kuwahara M, Iguchi K (2007) Occurrence of summer upstream migration in Biwa salmon (Oncorhynchus masou subsp.). Jpn J Ichthyol 54:15–20Google Scholar
  26. Kuwahara M, Maehata M, Akiyama H, Matsuda M, Okano T (1992) Fishes living in Yasu River. Ann Rep Biwako Bunkakan 10:47–61Google Scholar
  27. Kuwahara M, Maehata M, Akiyama H, Matsuda M, Okano T (1993) Fishes living in Ado River. Ann Rep Biwako Bunkakan 11:11–21Google Scholar
  28. Kuwahara M, Maehata M, Akiyama H, Matsuda M, Okano T (1994) Fishes living in Echi River. Ann Rep Biwako Bunkakan 12:9–18Google Scholar
  29. Kuwahara M, Takahashi H, Kikko T, Kurumi S, Iguchi K (2012) Introgression of Oncorhynchus masou subsp. (Biwa salmon) genome into lake-run O. m. ishikawae (Amago salmon) introduced into Lake Biwa, Japan. Ichthyol Res 59:195–201Google Scholar
  30. Meirmans PG (2015) Seven common mistakes in population genetics and how to avoid them. Mol Ecol 24:3223–3231Google Scholar
  31. Morita K, Yamamoto S (2004) Consequences of riverine fragmentation by damming: rivers are corridors between forest and the sea. In: Maekawa K (ed) Ecology and evolution of salmon and trout. Bunichi Sougou Shuppan, Tokyo, pp 281–312Google Scholar
  32. Morita K, Yamamoto S, Hoshino N (2000) Extreme life history change of white-spotted char (Salvelinus leucomaenis) after damming. Can J Fish Aquat sci 57:1300–1306Google Scholar
  33. Morita K, Nagasawa T (2010) Latitudinal variation in the growth and maturation of masu salmon (Oncorhynchus masou) parr. Can J Fish Aquat sci 67:955–965Google Scholar
  34. Nakabo T (2009) Zoogeography of Taiwanese fishes. Korean J Ichthyol 21:311–321Google Scholar
  35. Nakano S, Taguchi S, Shibata Y, Furukawa T (1989) Satsukimasu Amago salmon: Oncorhynchus masou ishikawae In: Kawanabe K, Mizuno N (eds) Freshwater fishes of Japan. Yamakei, Tokyo, pp 169–178Google Scholar
  36. Nakano S, Maekawa K (1994) Charr with special reference to the life history change and damming. In: Goto A, Tsukamoto K, Maekawa K (eds) Diadromous freshwater fishes-life history and evolution. Tokaidaigaku Shuppannkai, Kanagawa, pp. 86–100Google Scholar
  37. Oohara I, Okazaki T (1996) Genetic relationship among three subspecies of Oncorhynchus masou determined by mitochondrial DNA sequence analysis. Zool Sci 13:189–198Google Scholar
  38. Oshima M (1957) Sakuramasu and Biwamasu. Nire Shobo, SapporoGoogle Scholar
  39. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  40. Shimizu T, Taniguchi N, Mizuno N (1993) An electrophoretic study of genetic differentiation of a Japanese freshwater goby, Rhinogobius flumineus. Jpn J Ichthyol 39:329–343Google Scholar
  41. Shimoda K, Nakano S, Yamamoto S (2002) Landlocking of anadromous white-spotted charr Salvelinus leucomaenis by damming. Jpn J Ichthyol 49:25–32Google Scholar
  42. Sugiwaka K, Kojima H (1984) Influence of individual density on smoltification in wild juvenile masu salmon (Oncorhynchus masou) in the Atsuta River. Scientific reports of the Hokkaido Fish Hatchery 39:19–37Google Scholar
  43. Takahashi H, Kondou T, Takeshita N, Hsu TH, Nishida M (2016) Evolutionary process of iwame, a markless form of the red-spotted masu salmon Oncorhynchus masou ishikawae, in the Ôno River, Kyushu. Ichthyol Res 63: 132–144Google Scholar
  44. Tazawa S, Kamata T (1969) 1. Study to rear the native trout. Showa 42 fiscal year annual report of Shiga Prefectural Samegai Trout Farm 11–20Google Scholar
  45. Tega T, Noguchi D, Sano T, Tanaka H, Kuwada T, Mito T (2012) Evaluation of genetic diversity and genetic relationship between red-spotted masu trout Oncorhynchus masou ishikawae and Biwa saimon O. m. subsp. Fish Genet Breed Sci 41:51–61Google Scholar
  46. Thorpe JE (1986) Age at first maturity in Atlantic salmon, Salmo salar: freshwater period influences and conflicts with smolting. Can Spec Publ Fish Aquat Sci 89:7–14Google Scholar
  47. Thorpe JE (1989) Developmental variation in salmonid populations. J Fish Biol 35:295–303Google Scholar
  48. Thorpe JE (1994) An alternative view of smolting salmonids. Aquaculture 121:105–113Google Scholar
  49. Utoh H (1976) Study of the mechanism of differentiation between the stream resident form and the seaward migratory form in Masu salmon Brevoort. 1. Growth and sexual maturity of precocious masu salmon parr. Bull Fac Fish Hokkaido Univ 26:321–326Google Scholar
  50. Vekemans X (2002) AFLP-SURV 1.0: a program for genetic diversity analysis with AFLP (and RAPD) population data. Université Libre de Bruxelles, Bruxelles. Accessed on 6 January 2018
  51. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Homes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414Google Scholar
  52. Watanabe K, Nishida M (2003) Genetic population structure of Japanese bagrid catfishes. Ichthyol Res 50:140–148Google Scholar
  53. Watanabe K, Mori S, Nishida M (2003) Genetic relationships and origin of two geographic groups of the freshwater threespine stickleback, ‘Hariyo’. Zool Sci 20:265–274Google Scholar
  54. Yamamoto S (1973) Fishing in the mountain streams of west Japan. Tsurinotomosha, OsakaGoogle Scholar
  55. Yamamoto S, Nakano S (1996) Growth and development of a bimodal length-frequency distribution during smolting in a wild population of white-spotted charr in northern Japan. J Fish Biol 48:101–104Google Scholar
  56. Yamamoto S, Morita K, Kitano S, Watanabe K, Koizumi I, Maekawa K, Takamura K (2004) Phylogeography of white-spotted charr (Salvelinus leucomaenis) inferred from mitochondrial DNA sequences. Zool Sci 21:229–240Google Scholar

Copyright information

© The Ichthyological Society of Japan 2018

Authors and Affiliations

  • Masayuki Kuwahara
    • 1
    Email author
  • Hiroshi Takahashi
    • 2
  • Takeshi Kikko
    • 3
  • Seiji Kurumi
    • 4
  • Kei’ichiro Iguchi
    • 5
  1. 1.Lake Biwa MuseumKusatsuJapan
  2. 2.National Fisheries UniversityShimonosekiJapan
  3. 3.Shiga Prefectural Fisheries and Management DivisionOtsuJapan
  4. 4.Takashima City Makino Junior High SchoolTakashimaJapan
  5. 5.Graduate School of Fisheries and Environmental SciencesNagasaki UniversityNagasakiJapan

Personalised recommendations