First report of natural hybridization between two yellowtails, Seriola quinqueradiata and S. lalandi

Abstract

We report here the first case of natural hybridization between two yellowtails, Seriola quinqueradiata and Seriola lalandi, based on AFLP and mtDNA sequence data. Analysis of AFLP data using Bayesian model-based clustering methods revealed that 25 of 28 suspected hybrids are F1 hybrids and the remaining three are backcrosses to S. lalandi. Analysis of the mtDNA sequence indicated that hybridization is highly directional, as the majority of the F1 hybrids were offspring of S. quinqueradiata males and S. lalandi females. Considering the recent rapid distributional shift of S. quinqueradiata, our data indicate the need for further investigation of ongoing hybridization.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Albert V, Jónsson B, Bernatchez L (2006) Natural hybrids in Atlantic eels (Anguilla anguilla, A. rostrata): evidence for successful reproduction and fluctuating abundance in space and time. Mol Ecol 15:1903–1916

    CAS  Article  Google Scholar 

  2. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622

    Article  Google Scholar 

  3. Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Bensch S, Åkesson M (2005) Ten years of AFLP in ecology and evolution: why so few animals? Mol Ecol 14:2899–2914

    CAS  Article  Google Scholar 

  5. Duchesne P, Bernatchez L (2002) AFLPOP: a computer program for simulated and real population allocation, based on AFLP data. Mol Ecol Notes 2:380–383

    CAS  Article  Google Scholar 

  6. Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Res 4:359–361

    Article  Google Scholar 

  7. 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

    CAS  Article  Google Scholar 

  8. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    CAS  Article  Google Scholar 

  9. Hoshino N (2017) Migration of the Japanese yellowtail Seriola quinqueradiata in Hokkaido. Hokusuishi-dayori 94:1–4

    Google Scholar 

  10. Iguchi J, Takashima Y, Namikoshi A, Yamashita M (2012) Species identification method for marine products of Seriola and related species. Fish Sci 78:197–206

    Article  Google Scholar 

  11. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    CAS  Article  Google Scholar 

  12. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. https://doi.org/10.1186/1471-2156-11-94

    Article  PubMed  PubMed Central  Google Scholar 

  13. Koyama T, Nakamoto M, Morishima K, Yamashita R, Yamashita T, Sasaki K, Kuruma Y, Mizuno N, Suzuki M, Okada Y, Ieda R, Uchino T, Tasumi S, Hosoya S, Uno S, Koyama J, Toyoda A, Kikuchi K, Sakamoto T (2019) A SNP in a steroidogenic enzyme is associated with phenotypic sex in Seriola fishes. Curr Biol 29:1901–1909.e8. https://doi.org/10.1016/j.cub.2019.04.069

    CAS  Article  PubMed  Google Scholar 

  14. Kubota H, Furukawa S, Watari S (2019) Stock assessment and evaluation for yellowtail Seriola quinqueradiata (fiscal year 2018). In: Marine fisheries stock assessment and evaluation for Japanese waters (fiscal year 2018/2019). Fisheries Agency and Fisheries Research and Education Agency of Japan, Tokyo and Yokohama, pp. 1364–1401. https://abchan.fra.go.jp/digests2018/details/201842.pdf

  15. 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

    CAS  Article  Google Scholar 

  16. Martinez-Takeshita N, Purcell CM, Chabot CL, Craig MT, Paterson CN, Hyde JR, Allen LG (2015) A tale of three tails: cryptic speciation in a globally distributed marine fish of the genus Seriola. Copeia 103:357–368

    Article  Google Scholar 

  17. Montanari SR, Hobbs JPA, Pratchett MS, Van Herwerden L (2016) The importance of ecological and behavioural data in studies of hybridisation among marine fishes. Rev Fish Biol Fisheries 26:181–198

    Article  Google Scholar 

  18. Nakabo T (2013) Fishes of Japan with pictorial keys to the species, 3rd edn. Tokai University Press, Tokyo

    Google Scholar 

  19. Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:847–859

    CAS  Article  Google Scholar 

  20. Potts WM, Henriques R, Santos CV, Munnik K, Ansorge I, Dufois F, Booth AJ, Kirchner C, Sauer WHH, Shaw PW (2014) Ocean warming, a rapid distributional shift, and the hybridization of a coastal fish species. Glob Change Biol 20:2765–2777

    Article  Google Scholar 

  21. 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 

  22. R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/. Accessed 20 January 2016

  23. Sassa C, Takahashi M, Konishi Y, Yoshimasa A, Tsukamoto Y (2020) The rapid expansion of yellowtail (Seriola quinqueradiata) spawning ground in the East China Sea is linked to increasing recruitment and spawning stock biomass. ICES J Mar Sci 77:581–592

    Article  Google Scholar 

  24. Shiraishi T, Ohshimo S, Yukami R (2010) Age, growth and reproductive characteristics of gold striped amberjack Seriola lalandi in the waters off western Kyushu, Japan. New Zeal J Mar Fresh 44:117–127

    CAS  Article  Google Scholar 

  25. Shiraishi T, Ohshimo S, Yukami R (2011) Age, growth and reproductive characteristics of yellowtail (Seriola quinqueradiata) caught in the waters off western Kyushu. Bull Jpn Soc Fish Oceanogr 75:1–8

    Google Scholar 

  26. Takahashi H, Toyoda A, Yamazaki T, Narita S, Mashiko T, Yamazaki Y (2017) Asymmetric hybridization and introgression between sibling species of the pufferfish Takifugu that have undergone explosive speciation. Mar Biol 164: 90. https://doi.org/10.1007/s00227-017-3120-2

    CAS  Article  Google Scholar 

  27. Takatsuki Y, Kuragano T, Shiga T, Bungi Y, Inoue H, Fujiwara H, Ariyoshi M (2007) Long-term trends in sea surface temperature adjacent to Japan. Sokko Jiho 74:S33–S87

    Google Scholar 

  28. Tian Y, Kidokoro H, Watanabe T, Igeta Y, Sakaji H, Ino S (2012) Response of yellowtail, Seriola quinqueradiata, a key large predatory fish in the Japan Sea, to sea water temperature over the last century and potential effects of global warming. J Mar Syst 91:1–10

    Article  Google Scholar 

  29. Yamano H, Sugihara K, Nomura, K (2011) Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophys Res Lett 38. https://doi.org/10.1029/2010GL046474

  30. Vähä JP, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72

    Article  Google Scholar 

  31. Vekemans X, Beauwens T, Lemaire M, Roldán-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151

    CAS  Article  Google Scholar 

  32. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucl Acids Res 23:4407–4414

    CAS  Article  Google Scholar 

  33. Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc Lond B 360:1847–1857

    CAS  Article  Google Scholar 

  34. Wirtz P (1999) Mother species–father species: unidirectional hybridization in animals with female choice. Anim Behav 58:1–12

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We wish to thank Hiroshi Terado, the captain of the fishing boat “Kanryou-maru,” for his cooperation and support of this study. We are also grateful to Takeshi Matsuoka, Takafumi Ito, and many recreational anglers for kindly providing genetic samples and to Yasuko Ino for her help in the laboratory. This work was supported in part by JSPS KAKENHI (Grant number 17H03629).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Hiroshi Takahashi.

Additional information

Publisher's Note

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

Electronic supplementary material

About this article

Verify currency and authenticity via CrossMark

Cite this article

Takahashi, H., Kurogoushi, T., Shimoyama, R. et al. First report of natural hybridization between two yellowtails, Seriola quinqueradiata and S. lalandi. Ichthyol Res 68, 139–144 (2021). https://doi.org/10.1007/s10228-020-00752-8

Download citation

Keywords

  • Amberjacks
  • Sea of Japan
  • Climate change
  • Rapid distributional shifts