Conservation Genetics

, Volume 11, Issue 6, pp 2343–2355 | Cite as

Genetic population structure and management units of the endangered Tokyo bitterling, Tanakia tanago (Cyprinidae)

  • Hitoshi Kubota
  • Katsutoshi Watanabe
  • Naoyuki Suguro
  • Masaaki Tabe
  • Kazuhiro Umezawa
  • Seiichi Watanabe
Research Article

Abstract

The Tokyo bitterling Tanakia tanago (Cyprinidae) was once found throughout the Kanto Plain, central Japan, but most of their habitats have been lost due to human activities such as urbanization and improvement of paddy fields. Subsequently, conservation efforts, including captive breeding and reintroduction, have been ongoing. However, the genetic relationships among populations of this species including captive and remnant wild populations have been uncertain and thus management units for this species have been unidentified. We examined the population differentiation among 12 populations, including four wild and eight captive populations, and their relative genetic diversities to assist in conservation management decisions. Phylogeographic analyses based on partial mitochondrial cytochrome b gene sequences and microsatellite polymorphisms revealed four geographically associated genetic groups in the populations. Northern Tochigi populations have diverged from other populations (0.77% of dA), likely stemming from allopatric fragmentation following a change in the route of the Naka River, which occurred during the middle of the Pleistocene epoch. Microsatellite analysis has revealed that the genetic diversity of each population is generally low, and that most of the populations have experienced genetic bottlenecks. For future in- and ex-situ conservation programs to succeed, the population structure and genetic variability of remnant populations need to be taken into consideration.

Keywords

Conservation Genetic diversity Genetic population structure Management unit Microsatellite mtDNA 

Notes

Acknowledgments

We are grateful to Yoshikazu Nagata for providing samples and to Tomoyuki Nakamura and Nobuhiko Akiyama for providing helpful information on this species. Carl Smith made constructive suggestions for improving the manuscript. Yasuko Shirai kindly provided unpublished information on RC microsatellite primers. We would also like to thank anonymous reviewers for helpful comments. The Boards of Education in Tochigi and Kanagawa Prefectures helped greatly in obtaining permissions to collect samples from live fish. We also thank Naomi Sakae, Yuko Imai, Maiko Tachibana and Kahori Sato for laboratory assistance. This research was partly funded by the Fisheries Research Agency of Japan.

References

  1. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, MaldenGoogle Scholar
  2. Alpers DL, Van Vuuren BJ, Arctander P et al (2004) Population genetics of the roan antelope (Hippotragus equines) with suggestions for conservation. Mol Ecol 13:1771–1784CrossRefPubMedGoogle Scholar
  3. Angers B, Bernatchez L (1998) Combined use of SMM and non-SMM methods to infer fine structure and evolutionary history of closely related brook charr (Salvelinus fontinalis, Salmonidae) populations from microsatellites. Mol Biol Evol 15:143–159Google Scholar
  4. Aoyama J, Watanabe S, Ishikawa S et al (2000) Are morphological characters distinctive enough to discriminate between two species of freshwater eels, Anguilla celebesensis and A. interioris? Ichthyol Res 47:157–161CrossRefGoogle Scholar
  5. Arai R (2003) Tanakia tanago. In: Ministry of Environment (ed) Threatened wildlife of Japan—Red Data book, 2nd edn. Japan Wildlife Research Center, Tokyo, pp 40–41 (in Japanese)Google Scholar
  6. Briscoe DA, Malpica JM, Robertson A et al (1992) Rapid loss of genetic variation in large captive populations of Drosophila flies: implications for the genetic management of captive populations. Conserv Biol 6:416–425CrossRefGoogle Scholar
  7. Busack C, Knudsen CM (2007) Using factorial mating designs to increase the effective number of breeders in fish hatcheries. Aquaculture 273:24–32CrossRefGoogle Scholar
  8. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Am J Hum Genet 19:233–257PubMedGoogle Scholar
  9. Chiba Prefectural Boards of Education (1996) 1993–1995 Reports of the protection, propagation and research programmes of the natural monument “Tanakia tanago”. Chiba Prefectural Boards of Education, Chiba (in Japanese)Google Scholar
  10. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefPubMedGoogle Scholar
  11. Dawson DA, Burland TM, Douglas A et al (2003) Isolaiton of microsatellite loci in the freshwater fish, the bitterling Rhodeus sericeus (Teleostei: Cyprinidae). Mol Ecol Notes 3:199–202CrossRefGoogle Scholar
  12. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  13. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  14. Falush D, Stephens M, Prichard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  15. Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) Version 3.62. Department of Genome Science, University of Washington, Seattle, WAGoogle Scholar
  16. Fiumera AC, Parker PG, Fuerst PA (2000) Effective population size and maintenance of genetic diversity in captive-bred populations of a Lake Victoria cichlid. Conserv Biol 14:886–892CrossRefGoogle Scholar
  17. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeGoogle Scholar
  18. Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752PubMedGoogle Scholar
  19. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318CrossRefPubMedGoogle Scholar
  20. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices, version 2.9.3. http://www2.unil.ch/popgen/softwares/fstat.htm
  21. Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372CrossRefPubMedGoogle Scholar
  22. Hartl D, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer Associates, SunderlandGoogle Scholar
  23. Iguchi K, Watanabe K, Nishida M (1999) Reduced mitochondrial DNA variation in hatchery populations of ayu (Plecoglossus altivelis) cultured for multiple generations. Aquaculture 178:235–243CrossRefGoogle Scholar
  24. Inoue JG, Miya M, Tsukamoto K et al (2000) Complete mitochondrial DNA sequence of the Japanese sardine, Sardinops melanostictus. Fish Sci 66:924–932CrossRefGoogle Scholar
  25. Jones RO, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Res 10:551–555CrossRefGoogle Scholar
  26. Kaizuka S, Koike K, Endo K, et al (eds) (2000) Regional geomorphology of the Japanese Islands, vol. 4 geomorphology of Kanto and Izu-Ogasawara. University of Tokyo Press, Tokyo (in Japanese)Google Scholar
  27. Kanoh Y (2000) Reproductive success associated with territoriality, sneaking, and grouping in male rose bitterlings, Rhodeus ocellatus (Pisces: Cyprinidae). Environ Biol Fish 57:143–154CrossRefGoogle Scholar
  28. Katano O, Nakamura T (2005) Theory and problems in conservation ecology. In: Katano O, Mori S (eds) The present and future of endangered freshwater fishes in Japan. Shinzan-sha, Tokyo, pp 313–327 (in Japanese)Google Scholar
  29. Knapen D, Knaepkens G, Bervoets L et al (2003) Conservation units based on mitochondrial, nuclear DNA variation among European bullhead populations (Cottus gobio L., 1758) from Flanders, Belgium. Conserv Genet 4:129–140CrossRefGoogle Scholar
  30. Kubota H, Watanabe K (2003) Genetic diversity in wild and reared populations of the Japanese bitterling Tanakia tanago (Cyprinidae). Ichthyol Res 50:123–128CrossRefGoogle Scholar
  31. Kubota H, Watanabe K, Kakehi Y et al (2008) An assessment of genetic diversity in wild and captive populations of the endangered Japanese bitterling, Tanakia tanago (Cyprinidae) using amplified fragment length polymorphism (AFLP) markers. Fish Sci 74:494–502CrossRefGoogle Scholar
  32. Latch EK, Dharmarajan G, Glaubitz JC et al (2006) Relative performance of Bayesian clustering software for inferring population structure and individual assignment at low levels of population differentiation. Conserv Genet 7:295–302CrossRefGoogle Scholar
  33. Maehata M (1997) Circumstances and problems in preservation at aquarium. In: Nagata Y, Hosoya K (eds) Circumstances in endangered Japanese freshwater fishes and their protection. Midori-shobo, Tokyo, pp 205–217 (in Japanese)Google Scholar
  34. Minch E, Ruiz-Linares A, Goldstein D, et al (1996) Microsat (ver. 1.5): a computer program for calculating various statistics on microsatellite allele data. Stanford University Medical Center, Stanford, CA. http://hpgl.staford.edu/projects/microsat/microsat.html
  35. Mochizuki K (1997) Tanakia tanago. In: Nagata Y, Hosoya K (eds) Circumstances in endangered Japanese freshwater fishes and their protection. Midori-shobo, Tokyo, pp 64–75 (in Japanese)Google Scholar
  36. Mochizuki K, Kohno H, Taki Y (1998) Tanakia tanago. In: Fisheries Agency in Japan (ed) Data book of rare wild aquatic organisms in Japan. Japan Fisheries Resource Conservation Agency, Tokyo, pp 116–117 (in Japanese)Google Scholar
  37. Moritz C (1994) Defining ‘Evolutionary Significant Units’ for conservation. Trends Ecol Evol 9:373–375CrossRefGoogle Scholar
  38. Nakamura M (1969) Cyprinid fishes of Japan. Research Institute of Natural Resources, Tokyo (in Japanese)Google Scholar
  39. Nakamura T (1998) Natural conservation area of Tanakia tanago. In: Mori S (ed) Freshwater environment from a viewpoint of fish ecology. Shinzan-Sha Sci-Teck, Tokyo, pp 51–60 (in Japanese)Google Scholar
  40. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  41. Oda N (2005) Tanakia tanago. In: Katano O, Mori S (eds) The present and future of endangered freshwater fishes. Shinzansha, Tokyo, pp 168–176 (in Japanese)Google Scholar
  42. Perez-Enriquez R, Takagi M, Taniguchi N (1999) Genetic variability and pedigree tracing of a hatchery-reared stock of red sea bream (Pagrus major) used for stock enhancement, based on microsatellite DNA markers. Aquaculture 173:413–423CrossRefGoogle Scholar
  43. Posada D, Crandall KA, Templeton AR (2000) GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9:487–488CrossRefPubMedGoogle Scholar
  44. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  45. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249Google Scholar
  46. Reichard M, Smith C, Jordan WC (2004) Genetic evidence reveals density-dependent mediated success of alternative mating behaviours in the European bitterling (Rhodeus sericeus). Mol Ecol 13:1569–1578CrossRefPubMedGoogle Scholar
  47. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  48. Rowe G, Beebee TJC (2007) Defining population boundaries: use of three Bayesian approaches with microsatellite data from British natterjack toads (Bufo calamita). Mol Ecol 16:785–796CrossRefPubMedGoogle Scholar
  49. Saccheri I, Kuussaari M, Kankare M et al (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494CrossRefGoogle Scholar
  50. Schneider S, Roessli D, Excoffier L (2001) ARLEQUIN, version 2.001: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  51. Sekino M, Saitoh K, Yamada T et al (2003) Microsatellite-based pedigree tracing in a Japanese flounder Paralichthys olivaceus hatchery strain: implications for hatchery management related to stock enhancement program. Aquaculture 221:255–263CrossRefGoogle Scholar
  52. Shirai Y, Ikeda S, Tajima S (2009) Isolation and characterization of new microsatellite markers for rose bitterlings, Rhodeus ocellatus. Mol Ecol Res 9:1031–1033CrossRefGoogle Scholar
  53. Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264CrossRefPubMedGoogle Scholar
  54. Suguro N (2005) Bitterlings. In: Takashima F, Murai M (eds) Systems of aquaculture and fisheries enhancement. Freshwater fishes. Kouseisha-Kouseikaku, Tokyo, pp 171–183 (in Japanese)Google Scholar
  55. Takehana Y, Nagai N, Matsuda M et al (2003) Geographic variation and diversity of the cytochrome b gene in Japanese wild populations of medaka, Oryzias latipes. Zool Sci 20:1279–1291CrossRefPubMedGoogle Scholar
  56. Templeton AR (1998) Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 7:381–397CrossRefPubMedGoogle Scholar
  57. Templeton AR, Boerinkle E, Sing CF (1987) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics 117:343–351PubMedGoogle Scholar
  58. Tzika AC, Remy C, Gibson R, Milinkovitch MC (2009) Molecular genetic analysis of a captive-breeding program: the vulnerable endemic Jamaican yellow boa. Conserv Genet 10:69–77CrossRefGoogle Scholar
  59. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  60. Wang J (2009) A new method for estimating effective population sizes from a single sample of multilocus genotypes. Mol Ecol 18:2148–2164CrossRefPubMedGoogle Scholar
  61. Watanabe K, Takahashi H, Kitamura A et al (2006) Biogeographical history of Japanese freshwater fishes: Phylogeographic approaches and perspectives. Jpn J Ichthyol 53:1–38 (in Japanese with English summary)Google Scholar
  62. Watanabe K, Kano Y, Takahashi H et al (2010) GEDIMAP: a database of genetic diversity for Japanese freshwater fishes. Ichthyol Res 57:107–109CrossRefGoogle Scholar
  63. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  64. Zardoya R, Doadrio I (1999) Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids. J Mol Evol 49:227–237CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Hitoshi Kubota
    • 1
  • Katsutoshi Watanabe
    • 2
  • Naoyuki Suguro
    • 3
  • Masaaki Tabe
    • 4
  • Kazuhiro Umezawa
    • 5
  • Seiichi Watanabe
    • 6
  1. 1.Tochigi Prefectural Fisheries Experimental StationOhtawaraJapan
  2. 2.Department of Zoology, Graduate School of ScienceKyoto UniversitySakyoJapan
  3. 3.Freshwater Fisheries Experiment StationKanagawa Prefectural Fisheries Technology CenterSagamiharaJapan
  4. 4.Baika High SchoolToyonakaJapan
  5. 5.Department of Agriculture and ForestrySaitama PrefectureSaitamaJapan
  6. 6.Department of Marine BioscienceTokyo University of Marine Science and TechnologyMinatoJapan

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