Skip to main content

Advertisement

SpringerLink
Log in

Genetic characteristics of the amphidromous fish Ayu Plecoglossus altivelis altivelis (Osmeriformes: Plecoglossidae) on Yaku-shima Island in Japan, the southernmost population of the subspecies

  • Original Paper
  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The Ayu (Plecoglossus altivelis altivelis) population on Yaku-shima Island, Kagoshima Prefecture, Japan represents the southernmost population of the subspecies and is considered to be facing extinction. We investigated the genetic characteristics of Ayu in the Miyanoura River (MYU) in the northeast of the island and the Kurio River (KRO) in the southwest of the island, using partial sequences of mitochondrial (mt) control region and polymorphic microsatellite (simple sequence repeat: SSR) loci. The mtDNA analysis revealed that the Yaku-shima Island population was significantly differentiated from other Ayu populations; additionally, the MYU and KRO populations were significantly different from each other in terms of mtDNA (pairwise ΦST = 0.5826, P < 0.01) and SSR (pairwise ΦST = 0.1598, P < 0.01) analyses, indicating very little or no gene flow between them. The mtDNA haplotype diversity values were minimal for KRO and somewhat lower for MYU (h = 0.8176) than for each population from the mainland of Japan (Honshu–Kyushu) and the Korean Peninsula (h = 0.9905–1.0000). The mean values of expected heterozygosity (He) of SSRs were also lower in KRO (mean He = 0.555) than in MYU (mean He = 0.649). A considerably small effective population size (Ne = 100.1 for MYU, 151.2 for KRO) and a bottleneck effect for Yaku-shima Island population were suggested by SSR analysis. These findings underscore the importance of monitoring the genetic diversity of Ayu on Yaku-shima Island and the necessity of designing conservation policies for each river's population.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Abe S, Iguchi K, Nagumo T, Katano O (2005) Distribution of ayu (Plecoglossus altivelis) and benthic algal flora in the Yaku Island, Kagoshima Prefecture, Japan. Jpn J Phycol 53:1–5

    Google Scholar 

  • Aritomi A, Andou E, Yonezawa T, Kume G (2017) Monthly occurrence and feeding habits of larval and juvenile Ryukyu-ayu Plecoglossus altivelis ryukyuensis in an estuarine lake and coastal area of the Kawauchi River, Amami-oshima Island, southern Japan. Ichthyol Res 64:159–168

    Google Scholar 

  • Azuma M (1970) Studies on the variability of the landlocked Ayu-fish, Plecoglossus altivelis T et. S, in Lake Biwa. I. On the mode of distribution and some body form variation at early phases of development. Jpn J Ichthyol 20:63–76

    Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    CAS  PubMed  Google Scholar 

  • Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, Wohlfarth B, Mitrovica JX, Hostetler SW, McCabe AM (2009) The last glacial maximum. Science 325:710–714

    CAS  PubMed  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214

    CAS  PubMed  Google Scholar 

  • Ebise S, Nagafuchi O (2002) Runoff characteristics of water quality and influence of acid rain on mountainous streamwater on Yakushima Island. Jpn J Limnol 63:1–10

    CAS  Google Scholar 

  • 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 Res 10:564–567

    Google Scholar 

  • Excoffier L, Smouse PE, Quattro M (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fluxus Technology Ltd (2015) NETWORK ver 5.0. https://www.fluxus-engineering.com/sharenet_altwin.htm. Accessed 5 June 2020

  • Franklin IR (1980) Evolutionary change in small populations. In: Soulé ME, Wilcox BA (eds) Conservation biology: an evolutionary-ecological perspective. Sinauer Associates, Sunderland, pp 135–149

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    CAS  PubMed  Google Scholar 

  • Goudet L (2002) Fstat: a program to estimate and test gene diversities and fixation indices (ver.2.9.3.2). Institute of Ecology, University of Lausanne, Lausanne

    Google Scholar 

  • Han H-S, Taniguchi N, Lee J-H, Yoon M (2011) Genetic structure in wild populations of ayu Plecoglossus altivelis in Korea and Japan. Fish Aquat Sci 14:295–301

    CAS  Google Scholar 

  • Hosoya K (2013) Plecoglossidae. In: Nakabo T (ed) Fishes of Japan with pictorial keys to the species, 3rd edn. Tokai University Press, Hadano, pp 360, 1832

    Google Scholar 

  • Howes GJ, Sanford CPJ (1987) Oral ontogeny of the Ayu, Plecoglossus altivelis and comparisons with the jaws of other salmoniform fishes. Zool J Linn Soc 89:133–169

    Google Scholar 

  • Iguchi K, Nishida M (2000) Genetic biogeography among insular populations of the amphidromous fish Plecoglossus altivelis assessed from mitochondrial DNA analysis. Conserv Genet 1:147–156

    CAS  Google Scholar 

  • Iguchi K, Tanimura Y, Nishida M (1997) Sequence divergence in the mtDNA control region of amphidromous and landlocked forms of Ayu. Fish Sci 63:901–905

    CAS  Google Scholar 

  • Iguchi K, Tanimura Y, Takeshima H, Nishida M (1999) Genetic variation and geographic population structure of amphidromous Ayu Plecoglossu altivelis as examined by mitochondrial DNA sequencing. Fish Sci 65:63–67

    CAS  Google Scholar 

  • Ikeda M, Taniguchi N (2002) Genetic variation and divergence in populations of ayu Plecoglossus altivelis, including endangered subspecies, inferred from PCR-RFLP analysis of the mitochondrial DNA D-loop region. Fish Sci 68:18–26

    CAS  Google Scholar 

  • Ikeda M, Nunokawa M, Taniguchi N (2003) Lack of mitochondrial gene flow between populations of the endangered amphidromous fish Plecoglossus altivelis ryukyuensis inhabiting Amami-oshima Island. Fish Sci 69:1162–1168

    CAS  Google Scholar 

  • Iwata H, Watanabe K, Takeshima H, Iguchi K, Nishida M (2006) Isolation and characterization of 49 polymorphic microsatellite loci in the ayu, Plecoglossus altivelis. Mol Ecol Notes 6:1076–1079

    CAS  Google Scholar 

  • Jitousono T, Shimokawa E, Teramoto Y (2000) Rainfall and runoff of the Domen River in Yakushima Island. Res Bull Kagoshima Univ For 28:13–25

    Google Scholar 

  • Johnson WE, Koepfli K (2014) The role of genomics in conservation and reproductive sciences. In: Holt WV, Brown JL, Comizzoli P (eds) Reproductive sciences in animal conservation, progress and prospects. Springer, New York, pp 71–96

    Google Scholar 

  • Kano Y, Iida M, Tetsuka K, Saitoh T, Kato F, Sato T, Nishida S (2014) Effect of waterfalls on fluvial fish distribution and landlocked Rhinogobius brunneus populations on Yakushima Island, Japan. Ichthyol Res 61:305–316

    Google Scholar 

  • Katsumata Y, Uehara T, Ito H, Yoshimura J, Tainaka K, Ichinose G (2017) Territory holders and non-territory holders in Ayu fish coexist only in the population growth process due to hysteresis. Sci Rep. https://doi.org/10.1038/s41598-017-16859-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Kishino T, Shinomiya A (2003) Upstream migration of Ryukyu-ayu Plecoglossus altivelis ryukyuensis in the Yakugachi River, Amami-oshima Island, Japan. Nippon Suisan Gakkaishi 69:624–631

    Google Scholar 

  • Kishino T, Shinomiya A (2005) Migration and recruitment of amphidromous Ryukyu-ayu (Plecoglossus altivelis ryukyuensis) larvae and juveniles in Sumiyo and Yakeuchi Bays and neighboring waters, Amami-oshima Island, southern Japan. Jpn J Ichthyol 52:115–124

    Google Scholar 

  • Kishino T, Shinomiya A (2006) The behavior of Ryukyu-ayu Plecoglossus altivelis ryukyuensis larvae during downstream migration from the Yakugachi River flowing into Sumiyo Bay, Amami-oshima Island, southern Japan. Jpn J Ichthyol 53:143–149

    Google Scholar 

  • Kume G (2018) Occurrence of Ayu (Plecoglossus altivelis altivelis) in Yakushima Island. Occas Pap 59:95–96

    Google Scholar 

  • Kwan Y-S, Song H-K, Lee H-J, Lee W-O, Won Y-J (2012) Population genetic structure and evidence of demographic expansion of the Ayu (Plecoglossus altivelis) in East Asia. Anim Syst Evol Divers 28:279–290

    Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X ver 2.0. Bioinformatics 23:2947–2948

    CAS  Google Scholar 

  • Lonsinger RC, Adams JR, Waits LP (2018) Evaluating effective population size and genetic diversity of a declining kit fox population using contemporary and historical specimens. Ecol Evol 8:12011–12021

    PubMed  PubMed Central  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

    Google Scholar 

  • Maeno F (2014) What does caldera mean?: A example from the great Kikai eruption. Kagaku 84:58–63

    Google Scholar 

  • Maeno F, Taniguchi H (2005) Eruptive history of Satsuma Iwo-jima Island, Kikai Caldera, after a 6.5 ka caldera-forming eruption. Bull Volcanol Soc Jpn 50:71–85

    CAS  Google Scholar 

  • Maeno F, Taniguchi H (2007) Spatiotemporal evolution of a marine caldera-forming eruption, generating a low-aspect ratio pyroclastic flow, 7.3 ka, Kikai caldera, Japan: implication from near-vent eruptive deposits. J Volcanol Geotherm Res 167:212–238

    CAS  Google Scholar 

  • Ministry of Agriculture, Forestry and Fisheries (2020) The 93th statistical yearbook of Ministry of Agriculture, Forestry and Fisheries. Statistics Department, Ministry of Agriculture, Forestry and Fisheries, Tokyo. https://www.maff.go.jp/e/data/stat/93th/index.html. Accessed 24 Nov 2020

  • Ministry of the Environment, Government of Japan (2013) Threatened wildlife of Japan, red data book, 4th edn. Wildlife Research Center, Tokyo

    Google Scholar 

  • Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375

    CAS  PubMed  Google Scholar 

  • Nakabo T (2018) Family plecoglossidae. In: Nakabo T (ed) The natural history of the fishes of Japan. Shogakukan, Tokyo, pp 126–127

    Google Scholar 

  • Nakata T, Omoto K, Koba M (1978) Holocene emerged coral reef in Takarajima and Kodakarajima, Ryukyu Islands, southwest Japan. Sci Rep Tohoku Univ 7th ser Geogr 28:35–48

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    PubMed  Google Scholar 

  • Nishida M (1985) Substantial genetic differentiation in Ayu Plecoglossus altivelis of the Japan and Ryukyu Islands. Bull Jpn Soc Sci Fish 51:1269–1274

    Google Scholar 

  • Nishida M (1986) Geographic variation in the molecular, morphological and reproductive characters of the ayu Plecoglossus altivelis (Plecoglossidae) in the Japan-Ryukyu Archipelago. Jpn J Ichthyol 33:232–248

    Google Scholar 

  • Nishida M (1988) A new subspecies of the Ayu, Plecoglossus altivelis (Plecoglossidae) from the Ryukyu Islands. Jpn J Ichthyol 35:236–242

    Google Scholar 

  • Nishida M, Sawashi Y, Nishijima S, Azuma M, Fujimoto H (1992) Distribution and abundance of the Ryukyuan subspecies of the Ayu Plecoglossus altivelis ryukyuensis: results of a survey made in 1986. Nippon Suisan Gakkaishi 58:199–206

    Google Scholar 

  • Ota Y, Machida H, Hori N, Konishi K, Omura A (1978) Holocene raised coral reefs of Kikai-Jima (Ryukyu Islands)—an approach to Holocene sea level study. Geogr Rev Jpn 51:109–130

    Google Scholar 

  • Otake T, Yamada C, Uchida K (2002) Contribution of stocked ayu (Plecoglossus altivelis) to reproduction in the Nagara River, Japan. Fish Sci 68:948–950

    CAS  Google Scholar 

  • Palsbøll PJ, Bérubé M, Allendorf FW (2006) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16

    PubMed  Google Scholar 

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

    Google Scholar 

  • Polzin T, Daneshmand SV (2003) On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 31:12–20

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (ver 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

    PubMed  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for windows and Linux. Mol Ecol Resour 8:103–106

    PubMed  Google Scholar 

  • Sawashi Y, Nishida M (1994) Genetic differentiation in populations of the Ryukyu-ayu Plecoglossus altivelis ryukyuensis on Amami-oshima Island. Jpn J Ichthyol 41:253–260

    Google Scholar 

  • Sawashi Y, Fujimoto H, Azuma M, Nishijima S, Nishida M (1993) Genetic and morphological characteristics and distribution of the Ayu Plecoglossus altivelis in the northern Ryukyus. Nippon Suisan Gakkaishi 59:191–199

    Google Scholar 

  • Seki S, Taniguchi N, Jeon S-R (1988) Genetic divergence among natural populations of ayu from Japan and Korea. Nippon Suisan Gakkaishi 54:559–568

    CAS  Google Scholar 

  • Seki S, Agresti J, Gall GAE, Taniguchi N, May B (1999) AFLP analysis of genetic diversity in three populations of Ayu Plecoglossus altivelis. Fish Sci 65:888–892

    Google Scholar 

  • Senta T, Kinoshita I (1985) Larval and juvenile fishes occurring in surf zone of western Japan. Trans Am Fish Soc 114:609–618

    Google Scholar 

  • Shan X, Wu Y, Kang B (2005) Morphological comparison between Chinese Ayu and Japanese Ayu and establishment of Plecoglossus altivelis chinensis Wu & Shan subsp. nov. J Ocean Univ China 4:61–66

    Google Scholar 

  • Shields GF, Kocher TD (1991) Phylogenetic relationships of North American Ursids based on analysis of mitochondrial DNA. Evolution 45:218–221

    CAS  PubMed  Google Scholar 

  • Swatdipong A, Primmer CR, Vasemägi A (2010) Historical and recent genetic bottlenecks in European grayling, Thymallus thymallus. Conserv Genet 11:279–292

    Google Scholar 

  • Tachihara K (2018) Ryukyu-ayu. In: Nature Conservation Division, Department of Environmental Affairs, Okinawa Prefectural Government (ed) Threatened wildlife in Okinawa, 3rd edn (animals)—red data Okinawa. Nature Conservation Division, Department of Environmental Affairs, Okinawa Prefectural Government, Naha, p 231. https://www.pref.okinawa.jp/site/kankyo/shizen/hogo/okinawa_rdb_doubutu.html. Accessed 28 May 2019

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tajima F (1989b) The effect of change in population size on DNA polymorphism. Genetics 123:597–601

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takagi M, Shoji E, Taniguchi N (1999) Microsatellite DNA polymorphism to reveal genetic divergence in Ayu, Plecoglossus altivelis. Fish Sci 65:507–512

    CAS  Google Scholar 

  • Takahashi I, Azuma K, Hiraga H, Fujita S (1999) Different mortality in larval stage of Ayu Plecoglossus altivelis by birth dates in the Shimanto Estuary and adjacent coastal waters. Fish Sci 65:206–210

    CAS  Google Scholar 

  • Takeshima H, Iguchi K, Nishida M (2005) Unexpected ceiling of genetic differentiation in the control region of the mitochondrial DNA between different subspecies of the Ayu Plecoglossus altivelis. Zool Sci 22:401–410

    CAS  Google Scholar 

  • Takeshima H, Iguchi K, Hashiguchi Y, Nishida M (2016) Using dense locality sampling resolves the subtle genetic population structure of the dispersive fish species Plecoglossus altivelis. Mol Ecol 25:3048–3064

    PubMed  Google Scholar 

  • Tringali MD, Bert TM (1998) Risk to genetic effective population size should be an important consideration in fish stock-enhancement progress. Bull Mar Sci 62:641–659

    Google Scholar 

  • Ujiie H, Ujiie Y (1999) Late Quaternary course changes of the Kuroshio Curent in the Ryukyu Arc region, northwestern Pacific Ocean. Mar Micropaleontol 37:23–40

    Google Scholar 

  • Umitsu M (1991) Holocene sea-level changes and coastal evolution in Japan. Quat Res 30:187–196

    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

    Google Scholar 

  • Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262

    PubMed  Google Scholar 

Download references

Acknowledgements

Specimens were collected following the Kagoshima Prefectural rules and regulations. This work was supported by JSPS KAKENHI Grant Number 16K07827 and by Functional Enhancement Expenses in the Kagoshima University Operating Cost Grant "Advanced research infrastructure of biology and physiology of eel species inhabiting Southern Kyushu, Japan, Taiwan, and South East Asia and Creation of Industry-academia-government network to induce the social implementation of those research result".

Author information

Authors and Affiliations

  1. Graduate School of Fisheries and Environmental Sciences, Nagasaki University, 1-14 Bunkyo-machi, Nagasaki, 852-8521, Japan

    Naoki Yagishita

  2. Faculty of Fisheries, Kagoshima University, 4-50-20 Shimoarata, Kagoshima, 890-0056, Japan

    Gen Kume

Authors
  1. Naoki Yagishita
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gen Kume
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Naoki Yagishita.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 16 kb)

Supplementary file2 (DOCX 19 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yagishita, N., Kume, G. Genetic characteristics of the amphidromous fish Ayu Plecoglossus altivelis altivelis (Osmeriformes: Plecoglossidae) on Yaku-shima Island in Japan, the southernmost population of the subspecies. Genetica 149, 117–128 (2021). https://doi.org/10.1007/s10709-021-00117-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-021-00117-7

Keywords

Search

Navigation