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Fluctuating asymmetry in the insular population of ayu, Plecoglossus altivelis ryukyuensis, estimating its genetic diversity at extinction

Abstract

The present study tested the hypothesis that whether limited genetic diversity was the main factor that led the Ryukyu-ayu population on Okinawa-jima Island to extinction in the late 1970s. The usability of fluctuating asymmetry (FA) in reflecting genetic diversity was tested using two extant populations of Ryukyu-ayu on Amami-oshima Island, then used to estimate genetic diversity for the extinct population which only formalin-preserved specimens are available. The results showed that higher FA indices were associated with lower genetic diversity in the two extant populations, and the extinct population on Okinawa-jima Island had lower FA indices than the two extant populations on Amami-oshima Island. This finding suggests that the genetic diversity of the extinct population was not low enough as to cause its extinction.

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References

  1. 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

    Article  Google Scholar 

  2. Booy G, Hendriks RJJ, Smulders MJM, Van Groenendael JM, Vosman B (2000) Genetic diversity and the survival of populations. Plant Biol 2:379–395

    Article  Google Scholar 

  3. Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  4. Clarke GM, Brand GW, Whitten MJ (1986) Fluctuating asymmetry: a technique for measuring developmental stress caused by inbreeding. Aust J Biol Sci 39:145–153

    Article  Google Scholar 

  5. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140

    Article  Google Scholar 

  6. Ha ML, Iguchi K (2021) Geographical continuity and discontinuity in the meristic characteristics of ayus of the southern subspecies Plecoglossus altivelis ryukyuensis. Ichthyol Res 68:177–181

    Article  Google Scholar 

  7. 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

    Article  CAS  Google Scholar 

  8. 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  10. Iguchi K, Watanabe K, Nishida M (1999b) Reduced mitochondrial DNA variation in hatchery populations of ayu (Plecoglossus altivelis) cultured for multiple generations. Aquaculture 178:235–243

    Article  CAS  Google Scholar 

  11. Iguchi K, Watanabe K, Nishida M (2005) Validity of fluctuating asymmetry as a gauge of genetic stress in ayu stocks. Fish Sci 71:308–313

    Article  CAS  Google Scholar 

  12. 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 (In Japanese)

    Article  Google Scholar 

  13. Kishino T, Shinomiya A (2004) Appearance of upstream migrating individuals of Ryukyu-ayu Plecoglossus altivelis ryukyuensis at the Kawauchi and Yakugachi Rivers in Amami-oshima Island, Japan. Nippon Suisan Gakkaishi 70:179–186 (In Japanese)

    Article  Google Scholar 

  14. 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. Japan J Ichthyol 52:115–124 (In Japanese)

    Google Scholar 

  15. Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A 86:6196–6200

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  16. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  17. Leary RF, Allendorf FW (1989) Fluctuating asymmetry as an indicator of stress: implications for conservation biology. Trends Ecol Evol 4:214–217

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  18. Leary RF, Allendorf FW, Knudsen KL (1983) Developmental stability and enzyme heterozygosity in rainbow trout. Nature 301:71–72

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  19. Leary RF, Allendorf FW, Knudsen KL (1984a) Superior developmental stability of heterozygotes at enzyme loci in salmonid fishes. Am Nat 124:540–551

    Article  Google Scholar 

  20. Leary RF, Allendorf FW, Knudsen KL (1984b) Developmental stability of heterozygotes at enzyme loci in salmonid fishes. Biol Sci Fac Publ 124:540–551

    Google Scholar 

  21. Leary RF, Allendorf FW, Knudsen KL (1985a) Developmental instability as an indicator of reduced genetic variation in hatchery trout. Trans Am Fish Soc 114:230–235

    Article  Google Scholar 

  22. Leary RF, Allendorf FW, Knudsen KL (1985b) Inheritance of meristic variation and the evolution of developmental stability in rainbow trout. Evolution 39:308–314

    PubMed  Article  PubMed Central  Google Scholar 

  23. Leung B, Forbes MR, Houle D (2000) Fluctuating asymmetry as a bioindicator of stress: comparing efficacy of analyses involving multiple traits. Am Nat 155:101–115

    PubMed  Article  PubMed Central  Google Scholar 

  24. McCormack G (1998) Okinawan dilemmas: coral islands or concrete islands. In: JPRI Work. Pap. 45. https://openresearch-repository.anu.edu.au/bitstream/1885/41901/1/okinawan.html. Accessed 6 July 2020

  25. McDowall RM (1992) Diadromy: origins and definitions of terminology. Copeia 1992:248–251

    Article  Google Scholar 

  26. Murase I, Iguchi K (2019) Facultative amphidromy involving estuaries in an annual amphidromous fish from a subtropical marginal range. J Fish Biol 95:1391–1398

    PubMed  Article  PubMed Central  Google Scholar 

  27. Nakano Y, Kobari T, Yamaguchi A, Kume G (2020) Diet of the Ryukyu-ayu Plecoglossus altivelis ryukyuensis in subtropical rivers of Amami-oshima Island, southern Japan revealed by gut content analysis and inferred from stable isotope signatures. Japan J Ichthyol 67:287–292 (In Japanese)

    Google Scholar 

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

    Book  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  31. 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 (In Japanese)

    Article  Google Scholar 

  32. Oka S, Tokunaga K, Shinomiya A (1996) Feeding habit of larval and juvenile Ryukyu-ayu, Plecoglossus altivelis ryukyuensis in the surf zone of Sumiyo Bay, Amami-oshima Island. Japan J Ichthyol 43:21–26 (In Japanese)

    Google Scholar 

  33. Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Syst 17:391–421

    Article  Google Scholar 

  34. Parsons PA (1992) Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity 68:361–364

    PubMed  Article  PubMed Central  Google Scholar 

  35. R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  36. Reeve ECR (1960) Some genetic tests on asymmetry of sternopleural chaeta number in Drosophila. Genet Res 1:151–172

    Article  Google Scholar 

  37. Roldan ERS, Cassinello J, Abaigar T, Gomendio M (1998) Inbreeding, fluctuating asymmetry, and ejaculate quality in an endangered ungulate. Proc R Soc B 265:243–248

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  38. Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP v6: DNA sequence polymorphism analysis of large datasets. Mol Biol Evol 34:3299–3302

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  39. Shields G, Kocher T (1991) Phylogenetic relationship of North American ursids based on analysis mitochondrial DNA. Evolution 45:218–221

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  40. Tachihara K (2014) Plecoglossus altivelis ryukyuensis. In: Ministry of Environment (ed) Red data book 2014, threatened wildlife of Japan. Gyosei Corporation, Tokyo, pp 52–53 (In Japanese)

  41. 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. Zoolog Sci 22:401–410

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  42. Trokovic N, Herczeg G, Ghani NIA, Shikano T, Merilä J (2012) High levels of fluctuating asymmetry in isolated stickleback populations. BMC Evol Biol 12:115

    PubMed  PubMed Central  Article  Google Scholar 

  43. Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Book  Google Scholar 

  44. World Conservation Monitoring Centre (1996) Plecoglossus altivelis spp. ryukyuensis. The IUCN red list of threatened species 1996: e.T17595A7151908. https://doi.org/10.2305/IUCN.UK.1996.RLTS.T17595A7151908.en

  45. Yagishita N, Kume G (2021) 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

    PubMed  Article  CAS  PubMed Central  Google Scholar 

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Acknowledgments

We are grateful to the staff of the Okinawa Churaumi Research Center and Amami City, who provided fish samples for this research. The authors declare that the use of the fish specimens in the present study was performed in compliance with the current laws of Japan and the Guidelines for the use of fishes in research.

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Correspondence to Linh Manh Ha.

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Ha, L.M., Oka, Si. & Iguchi, K. Fluctuating asymmetry in the insular population of ayu, Plecoglossus altivelis ryukyuensis, estimating its genetic diversity at extinction. Ichthyol Res (2021). https://doi.org/10.1007/s10228-021-00840-3

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Keywords

  • Developmental instability
  • Endangered fish
  • Extinction risk
  • Population conservation
  • Ayu