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The genetic status of two subspecies of Rhodeus atremius, an endangered bitterling in Japan

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Abstract

Rhodeus atremius is an endemic bitterling fish from Japan comprising two endangered subspecies, R. a. atremius and R. a. suigensis. The latter subspecies, which had dramatically declined in last decades, was reported to contain two distinct mtDNA lineages. In order to estimate the optimized units for conservation management, the genetic structure of R. atremius was inferred by analyzing mtDNA and microsatellite markers (MS). Allelic richness and heterozygosity of MS in R. a. suigensis was less than half that in R. a. atremius. In R. a. suigensis, not only within-population genetic diversity but also among-population genetic divergence was low, with the exception of population Ah1, while the diversity was high and the divergence showed isolation by distance in R. a. atremius. In mtDNA and MS, R. a. suigensis concordantly formed a single lineage, while R. a. atremius encompassed four mtDNA lineages, two of which were completely admixed into one group on the basis of MS. In population Ah1 a striking introgression between the two subspecies was suggested by a Bayesian-based assignment test, with the presence of mtDNA haplotype of R. a. atremius. Contrary to the prevailing theory, R. a. suigensis corresponds to a single conservation unit, while three units seem appropriate for R. a. atremius. In addition, low genetic diversity of R. a. suigensis might have arisen mainly as a result of recent bottlenecks before population fragmentation, followed by current anthropogenic effects. Genetic introgression in population Ah1 was probably the result of human transplantation of R. a. atremius.

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References

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Auto Control 19:716–723

    Article  Google Scholar 

  • Allendorf FW, Luikart G (2006) Conservation and the genetics of populations. Blackwell, Malden, MA

    Google Scholar 

  • Arai R, Akai Y (1988) Acheilognathus melanogaster, a senior synonym of A. moriokae, with a revision of the genera of the subfamily Acheilognathinae (Cypriniformes, Cyprinidae). Bull Natl Sci Mus Tokyo Ser A 14:199–213

    Google Scholar 

  • Arai R, Fujikawa H, Nagata Y (2007) Four new subspecies of Acheilognathus bitterlings (Cyprinidae: Acheilognathinae) from Japan. Bull Nat Sci Mus Tokyo Ser A Suppl 1:1–28

    Google Scholar 

  • Asahida T, Kobayashi T, Saitoh K, Nakayama I (1996) Tissue preservation and total DNA extraction from fish stored at ambient temperature using buffers containing high concentration of urea. Fish Sci 62:727–730

    Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Bânârescu P (1990) Zoogeography of fresh waters, vol 1. AULA-Verlag, Wiesbaden

    Google Scholar 

  • Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58:445–449

    Article  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • Dawson DA, Burland TM, Douglas A, Comber SCL, Bradshaw M (2003) Isolation of microsatellite loci in the freshwater fish, the bitterling Rhodeus sericeus (Teleostei: Cyprinidae). Mol Ecol Notes 3:199–202

    Article  CAS  Google Scholar 

  • Degnan SM (1993) The perils of single gene trees—mitochondrial versus single-copy nuclear DNA variation in white-eyes (Aves: Zosteropidae). Mol Ecol 2:219–225

    Article  Google Scholar 

  • Di Rienzo A, Peterson AC, Garza JC et al (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170

    Article  PubMed  CAS  Google Scholar 

  • Earl DA, Louie KD, Bardeleben C, Swift CC, Jacobs DK (2010) Rangewide microsatellite phylogeography of the endangered tidewater goby, Eucyclogobius newberryi (Teleostei: Gobiidae), a genetically subdivided coastal fish with limited marine dispersal. Conserv Genet 11:103–114

    Article  Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa (L.) Skeels) endemic of Morocco. Theor Appl Genet 92:832–839

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • 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 131:479–491

    PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) ARLEQUIN version 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50

    CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Felsenstein J (2005) Phylogeny inference package (PHYLIP), version 3.65. University of Washington, Seattle, WA

    Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Froese R, Pauly D (2010) FishBase. http://www.fishbase.org/search.php. Cited 1 April 2010

  • Fujiwara H (1998) Search for the origin of rice cultivation. Iwanami Shoten, Tokyo, Japan

    Google Scholar 

  • Gompert Z, Nice CC, Fordyce JA, Forister ML, Shapiro AM (2006) Identifying units for conservation using molecular systematics: the cautionary tale of the Karner blue butterfly. Mol Ecol 15:1759–1768

    Article  PubMed  CAS  Google Scholar 

  • 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

  • Hashiguchi Y, Kado T, Kimura S, Tachida H (2006) Comparative phylogeography of two bitterlings, Tanakia lanceolata and T. limbata (Teleostei, Cyprinidae), in Kyushu and adjacent districts of Western Japan, based on mitochondrial DNA analysis. Zool Sci 23:309–322

    Article  PubMed  CAS  Google Scholar 

  • Hedrick PW (2010) Genetics of populations, 4th edn. Jones & Bartlett Publishers, Sudbury, MA

    Google Scholar 

  • Holsbeek G, Maes GE, Meester DE, Volckaert FAM (2009) Conservation of the introgressed European water frog complex using molecular tools. Mol Ecol 18:1071–1087

    Article  PubMed  CAS  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

    Google Scholar 

  • Kalinowski S (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Katano O, Mori S (2005) Distribution and ecology of endangered freshwater fishes. In: Katano O, Mori S (eds) The present and future of endangered freshwater fishes—scenario of fruitful conservation. Shinzansha, Tokyo, pp 1–10

    Google Scholar 

  • Kawamura K (2003) Rhodeus atremius suigensis. In: Ministry of the Environment (ed) Threatened wildlife of Japan. Red data book, 2nd edn, vol 4. Pisces: brackish and fresh water fishes. Japan wildlife research center, Tokyo, pp 46–47

  • Kawamura K (2005a) Low genetic variation and inbreeding depression in small isolated populations of the Japanese rosy bitterling, Rhodeus ocellatus kurumeus. Zool Sci 22:517–524

    Article  PubMed  CAS  Google Scholar 

  • Kawamura K (2005b) Values of Rhodeus atremius suigensis. In: Katano O, Mori S (eds) The present and future of endangered freshwater fishes—scenario of fruitful conservation. Shinzansha, Tokyo, pp 142–143

    Google Scholar 

  • Kawamura K, Ueda T, Arai R et al (2001) Genetic introgression by the rose bitterling, Rhodeus ocellatus ocellatus, into the Japanese rose bitterling, R. o. kurumeus (Teleostei: Cyprinidae). Zool Sci 18:1027–1039

    Article  CAS  Google Scholar 

  • Kawamura K, Katayama M, Miyake T et al (2009) Mechanisms of extinction of native species caused by exotic-related species. Jpn J Ecol 59:131–143

    CAS  Google Scholar 

  • Kimura S (2003) Rhodeus atremius atremius. In: Ministry of the Environment (ed) Threatened wildlife of Japan. Red data book, 2nd edn, vol 4. Pisces: brackish and fresh water fishes. Japan wildlife research center, Tokyo, pp 152–153

  • Konishi M, Hosoya K, Takata K (2003) Natural hybridization between endangered and introduced species of Pseudorasbora, with their genetic relationships and characteristics inferred from allozyme analyses. J Fish Biol 63:213–231

    Article  CAS  Google Scholar 

  • Kubota H, Watanabe K, Suguro N et al. (2010) Genetic population structure and management units of the endangered Tokyo bitterling, tanakia tanago (cyprinidae). Conserv Genet (in press). doi:10.1007/s10592-10010-10120-x

  • Leary RF, Allendorf FW, Forbes SH (1993) Conservation genetics of bull trout in the Columbia and Klamath River drainages. Conserv Biol 7:856–865

    Article  Google Scholar 

  • Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet J-M, Sherwin WB (1998a) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  PubMed  CAS  Google Scholar 

  • Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998b) Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol Ecol 7:963–974

    Article  PubMed  CAS  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • Masembe C, Muwanika VB, Nyakaana S, Arctander P, Siegismund HR (2006) Three genetically divergent lineages of the Oryx in eastern Africa: evidence for an ancient introgressive hybridization. Conserv Genet 7:551–562

    Article  CAS  Google Scholar 

  • Ministry of the Environment (2006) Law for the conservation of endangered species of wild fauna and flora, National endangered species of wild fauna and flora. http://www.env.go.jp/nature/yasei/hozonho/list_domestic.pdf. Cited 1 Jan 2010

  • Ministry of the Environment (2007) Biodiversity Center of Japan, Japan Integrated Biodiversity Information System. http://www.env.go.jp/press/file_view.php?serial=9944& hou_id=8648. Cited 1 Jan 2010

  • Miyake T, Kawamura K, Hosoya K, Okazaki T, Kitagawa T (2007) Discovery of the Japanese rosy bitterling, Rhodeus ocellatus kurumeus, in Nara Prefecture. Jpn J Ichthyol 54:139–148

    Google Scholar 

  • Miyake T, Nakajima J, Komaru A, Kawamura K (2008) Recent distribution of japanese rosy bitterling rhodeus ocellatus kurumeus in kyushu, inferred from mitochondrial DNA and morphology. Nippon Suisan Gakkaishi 74:1060–1067

    Article  CAS  Google Scholar 

  • Mori S, Katano O (2005) The problem and prospect of endangered freshwater fishes conservation. In: Katano O, Mori S (eds) The present and future of endangered freshwater fishes—scenario of fruitful conservation. Shinzansha, Tokyo, pp 13–31

    Google Scholar 

  • Moritz C (1994) Defining ‘Evolutionarily Significant Units’ for conservation. Trends Ecol Evol 9:373–375

    Article  PubMed  CAS  Google Scholar 

  • Murakami O, Washitani I (2002) Alien species and invasive alien species issues. In: The Ecological Society of Japan (ed) Handbook of alien species in Japan. Chijin-shokan, Tokyo, pp 3–4

  • Nagata Y (2002) Rhodeus atremius. In: Kawanabe H, Mizuno N, Hosoya K (eds) Freshwater fishes of Japan. Yamakei Press, Tokyo, pp 331, 360–366

  • Nagata Y, Fukuhara S (1998) Rhodeus atremius atremius. In: Fisheries Agency in Japan (ed) Basic data of rare wild aquatic organisms in Japan (V). Japan Fisheries Resource Conservation Association, Tokyo, pp 41–45, 50

  • Nakamura M (1969) Cyprinid fishes of Japan. Research Institute for Natural Resources, Tokyo

    Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  CAS  Google Scholar 

  • Neki A, Neki O (1997) Small ecology system of fishes in the area of water: way for irrigation, and the pernicious influence to this system by the improvement and its restoration: as a case study of the Okayama plains. Bull Nagaoka Univ Technol 19:141–150

    Google Scholar 

  • Okazaki M, Naruse K, Shima A, Arai R (2001) Phylogenetic relationships of bitterlings based on mitochondrial 12S ribosomal DNA sequences. J Fish Biol 58:89–106

    Article  CAS  Google Scholar 

  • Onikura N, Nakajima J, Eguchi K et al (2006) Change in distribution of bitterlings, and effects of urbanization on populations of bitterlings and unionid mussels in Tatara River system, Kyushu, Japan. J Jpn Soc Water Environ 29:837–842

    Article  CAS  Google Scholar 

  • Onikura N, Nakajima J, Eguchi K et al (2007) Relationships between the appearances and populations of freshwater fish species and the revetment conditions in the creeks around sea of Ariake, northwestern Kyushu island, Japan. J Jpn Soc Water Environ 30:277–282

    Article  Google Scholar 

  • Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP version 1.2: population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    PubMed  CAS  Google Scholar 

  • Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10

    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 

  • Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65

    Article  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  • Smith C, Reichard M, Jurajda P, Przybylski M (2004) The reproductive ecology of the European bitterling (Rhodeus sericeus). J Zool 262:107–124

    Article  Google Scholar 

  • Suzuki N (1995) Rhodeus atremius suigensis. In: Fisheries Agency in Japan (ed) Basic data of rare wild aquatic organisms in Japan (II). Japan Fisheries Resource Conservation Association, Tokyo, pp 308–313, 386

  • Suzuki N, Hibiya T (1984) Development of eggs and larvae of two bitterlings, Rhodeus atremius and R. suigensis (Cyprinidae). Jpn J Ichthyol 31:287–296

    Google Scholar 

  • Swofford AR (1999) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods), version 4.0. Sinauer, Sunderland

    Google Scholar 

  • Tabe M (1993) Genetic research of Rhodeus atremius suigensis in Ashida river. A School Board of Fukuyama, Hiroshima

    Google Scholar 

  • Taki Y (1993) History of earth told by fish. Gihodo Shuppan, Tokyo

    Google Scholar 

  • 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 4:535–538

    Article  Google Scholar 

  • Vrijenhoek RC (1998) Conservation genetics of freshwater fish. J Fish Biol 53(Supplement A):394–412

    Article  Google Scholar 

  • Waples RS (2002) Definition and estimation of effective population size in the conservation of endangered species. In: Beissinger SR, McCullough DR (eds) Population viability analysis. The University of Chicago Press, Chicago, pp 147–168

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wiepkema PR (1961) An ethological analysis of the reproductive behavior of the bitterling (Rhodeus amarus Bloch). Arch Neerl Zool 14:103–199

    Article  Google Scholar 

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Acknowledgments

We thank the staff of the Ministry of the Environment of Japan and Okayama Prefecture Environmental Conservation Agency for supplying samples of R. a. suigensis. We also thank Carl Smith (University of St. Andrews, UK) for comments and English revision. We express sincere thanks to two anonymous reviewers for the critical comments and useful suggestions that have helped us to improve our paper considerably. This study was carried out as a part of a conservation project for R. a. suigensis organized by the Ministry of Environment of Japan, the Fisheries Agency in Japan and Okayama Prefectural Office. This study was partly supported by Interdisciplinary Research Institute of Environmental Sciences.

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Correspondence to Kouichi Kawamura.

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See Tables 5 and 6

Table 5 Genetic characteristics of Rhodeus atremius atremius
Table 6 Genetic characteristics of Rhodeus atremius suigensis

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Miyake, T., Nakajima, J., Onikura, N. et al. The genetic status of two subspecies of Rhodeus atremius, an endangered bitterling in Japan. Conserv Genet 12, 383–400 (2011). https://doi.org/10.1007/s10592-010-0146-0

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