Skip to main content
Log in

The origins of limnetic forms and cryptic divergence in Gnathopogon fishes (Cyprinidae) in Japan

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

The cyprinid species of the genus Gnathopogon, exhibiting flexible morphological and ecological variation, include limnetic life forms. We examined the origin of the limnetic forms and the population divergence of the Japanese Gnathopogon species, using molecular phylogenetic and phylogeographic analyses. A Bayesian phylogenetic inference approach based on mtDNA cytochrome b sequence data revealed three major lineages in G. elongatus. One of them formed a monophyletic group with the limnetic species G. caerulescens, which is endemic to an ancient lake, Lake Biwa. The divergence of the G. caerulescens lineage was estimated to date back to the early Pleistocene. This precedes the formation of the extensive pelagic environment in the present Lake Biwa. However, the recent genetic divergence of G. caerulescens was inferred to originate in the present Lake Biwa in the late Pleistocene. Another lacustrine population in the Mikata Lakes was shown to belong to a different lineage from G. caerulescens. The majority of the population possessed unique, but non-monophyletic, haplotypes, suggesting a short evolutionary history. One of the cryptic lineages of G. elongatus discovered in the Ina Valley, the lower area of Lake Suwa, might be related to the extinct lacustrine subspecies G. elongatus suwae, which has been replaced by introduced congeners. The previous and ongoing introductions of Gnathopogon fishes would have produced genetic disturbance to the indigenous populations.

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

Access this article

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
Fig. 5

Similar content being viewed by others

References

  • Aoyama J, Watanabe S, Ishikawa S, Nishida M, Tsukamoto K (2000) Are morphological characters distinctive enough to discriminate between two species of freshwater eels, Anguilla celebesensis and A. interioris? Ichthyol Res 47:157–161

    Article  Google Scholar 

  • Bănărescu P, Nalbant TT (1973) Pisces, Teleostei, Cyprinidae (Gobioninae). Das Tierreich, Lieferung 93. Walter de Guryter, Berlin

  • Biodiversity Center of Japan (2002) The national survey on the natural environment report of the distributional survey of Japanese animals (freshwater fishes). Japan Wildlife Research Center, Tokyo

    Google Scholar 

  • Burridge CP, Craw D, Fletcher D, Waters JM (2008) Geological dates and molecular rates: fish DNA sheds light on time dependency. Mol Biol Evol 25:624–633

    Article  PubMed  CAS  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  PubMed  CAS  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed  Google Scholar 

  • Drummond AJ, Suchard MA (2010) Bayesian random local clocks, or one rate to rule them all. BMC Biol 8:114

    Article  PubMed  Google Scholar 

  • Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192

    Article  PubMed  CAS  Google Scholar 

  • Eschmeyer WN, Fricke R (2011) Catalog of Fishes electronic (version 5 May 2011). http://research.calacademy.org/ichthyology/catalog/fishcatmain.asp. Accessed 20 May 2011

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Froese R, Pauly D (2011) FishBase. World Wide Web electronic publication.http://www.fishbase.org. version 2011/2. Accessed 20 May 2011

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Harada S, Jeon SR, Kinoshita I, Tanaka M, Nishida M (2002) Phylogenetic relationships of four species of floating gobies (Gymnogobius) as inferred from partial mitochondrial cytochrome b gene sequences. Ichthyol Res 49:324–332

    Article  Google Scholar 

  • Hosoya K (1986) Interrelationships of the Gobioninae (Cyprinidae). In: Uyeno T, Arai R, Taniuchi T, Matsuura K (eds) Indo-Pacific fish biology: proceeding of the second international conference on indo-pacific fishes. Ichthyological Society of Japan, Tokyo, pp 484–501

    Google Scholar 

  • Hosoya K (1987) Phylogeny and character displacement in Gnathopogon fishes. In: Mizuno N, Goto A (eds) Freshwater fishes in Japan: their distribution, variation and speciation. Tokai University Press, Tokyo, pp 31–40 (in Japanese)

    Google Scholar 

  • Hosoya K (1997) The endangered Japanese freshwater fishes. In: Nagata Y, Hosoya K (eds) Circumstances in endangered Japanese freshwater fishes and their protection. Midori Shobo, Tokyo, pp 3–21 (in Japanese)

    Google Scholar 

  • Hosoya K (2000) Cyprinidae. In: Nakabo T (ed) Fishes of Japan with pictorial keys to the species, 2nd edn. Tokai University Press, Tokyo, pp 253–271 (in Japanese)

    Google Scholar 

  • Hosoya K (2001) Gnathopogon. In: Kawanabe H, Mizuno N, Hosoya K (eds) Freshwater fishes of Japan, 3rd edn. Yama-Kei Publishers, Tokyo, pp 297–299 (in Japanese)

    Google Scholar 

  • Hosoya K (2003) Gnathopogon elongatus suwae. In: (ed) Japan ministry of the environment. Threatened wildlife of Japan, red data book, 2nd edition. Japan Wildlife Research Center, Tokyo, pp 26–27 (in Japanese)

  • Jordan DS, Fowler HW (1903) A review of the cyprinid fishes of Japan. Proc U S Natn Mus 26(1334):811–862

    Article  Google Scholar 

  • Jordan DS, Hubbs CL (1925) Record of fishes obtained by David Starr Jordan in Japan, 1922. Mem Carneg Mus 10:93–346

    Google Scholar 

  • Kawabe T (1989) Stratigraphy of the lower part of the Kobiwako group around the Ueno Basin, Kinki District, Japan. J Geosci, Osaka City Univ 32:39–52

    Google Scholar 

  • Kawabe T (1994) Chapter 1. Biwako no Oitachi (formation of Lake Biwa). In: Research group for natural history of Lake Biwa (ed) Biwako no Shizenshi (The natural history of Lake Biwa). Yasaka Shobo, Tokyo, pp 24–72 (in Japanese)

  • Kawanabe H (1978) Some biological problems. Verh Internat Ver Limnol 20:2674–2677

    Google Scholar 

  • Kawanabe H (1996) Asian great lakes, especially Lake Biwa. Environ Biol Fish 47:219–234

    Article  Google Scholar 

  • Kohno N, Hosoe A, Ogawa S (2006) Species composition of fish caught by shore seine in Lake Kizaki. Bull Nagano Pref Fish Exp Stn 8:35–38 (in Japanese)

    Google Scholar 

  • Komiya T, Fujita S, Watanabe K (2011) A novel resource polymorphism in fish, driven by differential bottom environments: an example from an ancient lake in Japan. PLoS One 6:e17430

    Article  PubMed  CAS  Google Scholar 

  • Kontula T, Kirilchik SV, Vainola R (2003) Endemic diversification of the monophyletic cottoid fish species flock in Lake Baikal explored with mtDNA sequencing. Mol Phylogenet Evol 58:142–147

    Google Scholar 

  • Kornfield I, Smith PF (2000) African cichlid fishes: model systems for evolutionary biology. Annu Rev Ecol Syst 31:163–196

    Article  Google Scholar 

  • Kottelat M, Freyhof J (2007) Gobioninae. In: Kottelat M, Freyhof J (eds) Handbook of European freshwater fishes. Publications Kottelat, Cornol, pp 85–108

    Google Scholar 

  • Kurasawa H, Yamamoto M, Okino T (1981) Chronological changes of fish and mollusca faunae and transplantation species in Lake Suwa. Ann Environ Sci Shinshu Univ 3:1–6 (in Japanese)

    Google Scholar 

  • Machida H, Matsuda T, Umitsu M, Koizumi T (2006) Regional geomorphology of the Japanese Islands, vol 5: Geomorphology of Chubu. University of Tokyo Press, Tokyo

    Google Scholar 

  • Martens K (1997) Speciation in ancient lakes. Trends Ecol Evol 12:177–182

    Article  PubMed  CAS  Google Scholar 

  • Matsushima S (1995) Morphogenetic history of the Ina basin. Res Rep Iida City Mus 3:1–145 (in Japanese with English abstract)

    Google Scholar 

  • Mayden RL, Chen WJ, Bart HL, Doosey MH, Simons AM, Tang KL, Wood RM, Agnew MK, Yang L, Hirt MV, Clements MD, Saitoh K, Sado T, Miya M, Nishida M (2009) Reconstructing the phylogenetic relationships of the earth’s most diverse clade of freshwater fishes—order Cypriniformes (Actinopterygii: Ostariophysi): a case study using multiple nuclear loci and the mitochondrial genome. Mol Phylogenet Evol 51:500–514

    Article  PubMed  CAS  Google Scholar 

  • Meyers PA, Takemura K, Horie S (1993) Reinterpretation of late Quaternary sediment chronology of Lake Biwa, Japan, from correlation with marine glacial–interglacial cycles. Quat Res 39:154–162

    Article  Google Scholar 

  • Miyadi D (1930) Kizaki-Ko no gyorui ni tsuite (On fishes of Lake Kizaki). In: Tanaka A (ed) Nippon Kita-Alps Kosho no Kenkyu (Studies on the lakes of Japanese Northern Alps). Shinano Kyoiku-Kai Kitaazumi Bukai, Omachi, pp 626–630 (in Japanese)

    Google Scholar 

  • Moriyama A (2001) Chronology of mountain formation in the Central Mountain region in Japan. In: Yonekura N, Okada A, Moriyama A (eds) Hendou Chikeigaku (Techtonic geomorphology). Kokinshoin, Tokyo, pp 87–109 (in Japanese)

    Google Scholar 

  • Nakajima T (1994) Chapter 4-d. Cyprinid fishes. In: Research group for natural history of Lake Biwa (ed) Biwako no Shizenshi (The natural history of Lake Biwa), Yasaka Shobo, Tokyo, pp 235–275 (in Japanese)

  • Nakamura M (1969) Cyprinid Fishes of Japan. Spec Publ Res Inst Nat Resour, Tokyo (in Japanese)

  • Okada Y, Nakamura M (1948) Zoshoku (Aquaculture). In: Nippon no Tansui-Gyorui (Freshwater fishes of Japan), Nippon Shuppan-sha, Osaka, pp 119–125 (in Japanese)

  • Palumbi S, Martin A, Romano S, McMillian WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. University of Hawaii, Honolulu

    Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitutions. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Rambaut A (2009) FigTree Version 1.3.1. http://tree.bio.ed.ac.uk/software/figtree/

  • Rambaut A, Drummond AJ (2009) Tracer version 1.5. http://tree.bio.ed.ac.uk/software/tracer/

  • Saitoh K, Miya M, Inoue JG, Ishiguro NB, Nishida M (2003) Mitochondrial genomics of ostariophysan fishes: perspectives on phylogeny and biogeography. J Mol Evol 56:464–472

    Article  PubMed  CAS  Google Scholar 

  • Saitoh K, Sado T, Mayden RL, Hanzawa N, Nakamura K, Nishida M, Miya M (2006) Mitogenomic evolution and interrelationships of the Cypriniformes (Actinopterygii: Ostariophysi): The first evidence towards resolution of higher-level relationships of the world. J Mol Evol 63:826–841

    Article  PubMed  CAS  Google Scholar 

  • Saitoh K, Sado T, Doosey MH, Bart HL Jr, Inoue JG, Nishida M, Mayden RL, Miya M (2011) Evidence from mitochondrial genomics supports the lower Mesozoic of South Asia as the time and place of basal divergence of cypriniform fishes (Actinopterygii: Ostariophysi). Zool J Linn Soc 161:633–662

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sakai H (1995) Natural hybrid and speciation in fish. Biol Sci 47:113–123 (in Japanese)

    Google Scholar 

  • Schluter D (1998) Ecological speciation in postglacial fishes. In: Grant PR (ed) Evolution on islands. Oxford University Press, Oxford

    Google Scholar 

  • Schluter D, McPhail JD (1992) Ecological character displacement and speciation in sticklebacks. Am Nat 140:85–108

    Article  PubMed  CAS  Google Scholar 

  • Snorrason SS, Skúlason S, Jonsson B, Malmquist HJ, Jónasson PM, Sandlund OT, Lindem T (1992) Trophic specialization in Arctic charr Salvelinus alpinus (Pisces; Salmonidae): morphological divergence and ontogenetic niche shifts. Biol J Linn Soc 52:1–18

    Article  Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), ver 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Takahashi S (1989) A review of the origins of endemic species in Lake Biwa with special reference to the goby fish, Chaenogobius isaza. J Paleolimnol 1:279–292

    Article  Google Scholar 

  • Takei K (2007) Verified the list of the fishes of Lake Suwa. Bull Nagano Pref Fish Exp Stn 9:7–21 (in Japanese)

    Google Scholar 

  • Takemura K, Kitagawa H, Hayashida A, Yasuda Y (1994) Sedimentary facies and chronology of core samples from Lake Mikata, Lake Suigetsu and Kurota Lowland, central Japan—sedimentary environment in Mikata Lowland since the last interglacial time. J Geography 103:233–242

    Article  Google Scholar 

  • Tang KL, Agnew MK, Chen WJ, Vincent Hirt M, Raley ME, Sado T, Schneider LM, Yang L, Bart HL, He S, Liu H, Miya M, Saitoh K, Simons AM, Wood RM, Mayden RL (2011) Phylogeny of the gudgeons (Teleostei: Cyprinidae: Gobioninae). Mol Phylogenet Evol 61:103–124

    Article  PubMed  Google Scholar 

  • Temminck CJ, Schlegel H (1846) Pisces. Fauna Japonica, sive descriptio animalium quae in itinere per Japoniam suscepto annis 1823–30 collegit, notis observationibus et adumbrationibus illustravit P. F. de Siebold. Parts 10–14:173–269

    Google Scholar 

  • Tokui T, Kawanabe H (1984) Fishes. In: Horie S (ed) Lake Biwa, monographiae biologicae (volume 54). Dr W Junk Publishers, Dordrecht, pp 339–360

    Google Scholar 

  • Tomoda Y (1978) Biwako to Namazu (Lake Biwa and catfish). Chobunsha, Tokyo (in Japanese)

    Google Scholar 

  • Watanabe K (1998) Parsimony analysis of the distribution pattern of Japanese primary freshwater fishes, and its application to the distribution of the bagrid catfishes. Ichthyol Res 45:259–270

    Article  Google Scholar 

  • Watanabe K (2010) Faunal structure of Japanese freshwater fishes and its artificial disturbance. Environ Biol Fish. doi:10.1007/s10641-010-9601-5

  • Watanabe K, Takahashi H (2010) Tansuigyorui chiri no shizenshi (Natural history of freshwater fish geography). Hokkaido University Press, Sapporo (in Japanese)

    Google Scholar 

  • Watanabe K, Iguchi K, Hosoya K, Nishida M (2000) Phylogenetic relationships of the Japanese minnows, Pseudorasbora (Cyprinidae), as inferred from mitochondrial 16 S rRNA gene sequences. Ichthyol Res 47:43–50

    Article  Google Scholar 

  • Watanabe K, Kano Y, Takahashi H, Mukai T, Kakioka R, Tominaga K (2010) GEDIMAP: a database of genetic diversity for Japanese freshwater fishes. Ichthyol Res 57:107–109

    Article  Google Scholar 

  • Winfield IJ, Nelson JS (1991) Cyprinid fishes: systematics, biology and exploitation. Chapman & Hall, London

    Book  Google Scholar 

  • Yada T (1977) Studies on the spawning period and number of egg spawned on “Tamoroko”, Gnathopogon elongatus elongatus. Bull Osaka Pref Freshwater Fish Exp Stn 5:1–8 (in Japanese)

    Google Scholar 

  • Yang JQ, He SP, Freyhof J, Witte K, Liu HZ (2006) The phylogenetic relationships of the gobioninae (Teleostei: Cyprinidae) inferred from mitochondrial cytochrome b gene sequences. Hydrobiologia 553:255–266

    Article  CAS  Google Scholar 

  • Yokoyama T (1984) Stratigraphy of the quaternary system around Lake Biwa and geohistory of the ancient Lake Biwa. In: Horie S (ed) Lake Biwa, monographiae biologicae (volume 54). Dr W Junk Publishers, Dordrecht, pp 43–128

    Google Scholar 

  • Yokoyama T (1988) Seinan Nihon no Shizenshi (Natural history of southwestern Japan). Sanwa-shobo, Kyoto (in Japanese)

    Google Scholar 

  • Yonekura N, Kaizuka S, Nogami M, Chinzai K (2001) Regional geomorphology of the Japanese Islands, vol 1: introduction to Japanese geomorphology. University of Tokyo Press, Tokyo (in Japanese)

    Google Scholar 

  • Yuma H, Hosoya K, Nagata Y (1998) Distribution of the freshwater fishes of Japan: an historical overview. Environ Biol Fish 52:97–124

    Article  Google Scholar 

Download references

Acknowledgments

We are very grateful to T. Abe, T. Asaka, T. Karube, K. Kodama, T. Komiya, H. Kumada, T. Mukai, H. Ogawa, H. Sakai, M. Sugimura, N. Suzuki, and K. Tominaga for providing a portion of specimen, M. Nishida for lending us experimental instruments, and K. Hosoya for giving us valuable information. This study was partly supported by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan (nos. 18570086, 21370035, and 2155282, and “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem” of the GCOE).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Ryo Kakioka or Katsutoshi Watanabe.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 31 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kakioka, R., Kokita, T., Tabata, R. et al. The origins of limnetic forms and cryptic divergence in Gnathopogon fishes (Cyprinidae) in Japan. Environ Biol Fish 96, 631–644 (2013). https://doi.org/10.1007/s10641-012-0054-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-012-0054-x

Keywords

Navigation