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Microsatellite DNA variation of oval squid Sepioteuthis sp. 2 reveals a single fishery stock on the coastline of mainland Japan

Abstract

The level of genetic diversity and population differentiation of oval squid Shiro-ika Sepioteuthis sp. 2 around mainland Japan were examined using highly polymorphic DNA markers. Ten microsatellite loci showed relatively low genetic diversity (average observed heterozygosity H O = 0.68, overall mean number of alleles N A = 10.0) as compared with other squid, which may be explained by a recent history of population expansion. Populations from 12 sites along the coastline of Japan were genetically homogeneous, as measured by F ST values (global F ST: −0.0006; pairwise F ST: from −0.0046 to 0.0083), R ST values (global R ST: 0.0025; pairwise R ST: from −0.0076 to 0.03), a neighbor-joining (NJ) tree based on Cavalli-Sforza and Edwards chord distance, Bayesian clustering or analyses of three geographical groups (Sea of Japan, Seto Inland Sea, and Pacific Ocean; F CT = −0.0005), and should be considered as a single fishery stock. Allele frequencies also showed a high degree of similarity across different years in the samples taken from Hiroshima. Factors influencing this homogeneity include genetic exchange without barriers preventing gene flow, larval dispersal, and active adult migration of Sepioteuthis sp. 2.

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References

  1. 1.

    Jereb P, Roper CFE (eds) (2010) Cephalopods of the world: an annotated and illustrated catalogue of species known to date, vol 2. Myopsid and oegopsid squid. FAO Species Catalogue for Fishery Purpose. No. 4. FAO, Rome

  2. 2.

    Okutani T (1984) Life history of the oval squid, Sepioteuthis lessoniana. Saibai Giken 13:69–75 (In Japanese)

  3. 3.

    Segawa S, Hirayama S, Okutani T (1993) Is Sepioteuthis lessoniana in Okinawa a single species? In: Okutani T, O’Dor RK, Kubodera T (eds) Recent advance in fisheries biology. Tokai University Press, Tokyo, pp 513–521

  4. 4.

    Segawa S, Izuka T, Tamashiro T, Okutani T (1993) A note on mating and egg deposition by Sepioteuthis lessoniana in Ishigaki Island, Okinawa, southwestern Japan. Jpn J Malacol Venus 52:195–207

  5. 5.

    Izuka T, Segawa S, Okutani T, Numachi K (1994) Evidence on the existence of three species in the oval squid Sepioteuthis lessoniana complex in Ishigaki Island, Okinawa, southwestern Japan, by isozyme analyses. Jpn J Malacol Venus 53:217–228

  6. 6.

    Izuka T, Segawa S, Okutani T (1996) Biochemical study of the population heterogeneity and distribution of the oval squid Sepioteuthis lessoniana complex in southwestern Japan. Am Malacol Bull 12:129–135

  7. 7.

    Imai H, Aoki M (2012) Genetic diversity and genetic heterogeneity of bigfin reef squid “Sepioteuthis lessoniana” species complex in northwestern Pacific Ocean. In: Caliskan Mahmut (ed) Analysis of genetic variation in animals. InTech, Croatia, pp 151–166

  8. 8.

    Yokogawa K, Ueta Y (2000) Genetic analysis of oval squid (Sepioteuthis lessoniana) around Japan. Jpn J Malacol Venus 59:45–55

  9. 9.

    Aoki M, Imai H, Naruse T, Ikeda Y (2008) Low genetic diversity of oval squid, Sepioteuthis cf. lessoniana (Cephalopoda: Loliginidea), in Japanese waters inferred from a mitochondrial DNA non-coding region. Pac Sci 62:403–411

  10. 10.

    Garoia F, Guarniero I, Ramsak A, Ungaro N, Landi M, Piccinetti C, Mannini P, Tinti F (2004) Microsatellite DNA variation reveals high gene flow and panmictic populations in the Adriatic shared stocks of the European squid and cuttlefish (Cephalopoda). Heredity 93:166–174

  11. 11.

    Shaw PW, Arkhipkin AI, Adcock GJ, Burnett WJ, Carvalho GR, Scherbich JN, Villegas PA (2004) DNA markers indicate that distinct spawning cohorts and aggregations of Patagonian squid, Loligo gahi, do not represent genetically discrete subpopulations. Mar Biol 144:961–970

  12. 12.

    Shaw PW, Pierce GJ, Boyle PR (1999) Subtle population structuring within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Mol Ecol 8:407–417

  13. 13.

    Shaw PW, Hendrickson L, McKeown NJ, Stoiner T, Naud MJ, Sauer WHH (2010) Discrete spawning aggregations of loliginid squid do not represent genetically distinct populations. Mar Ecol Prog Ser 408:117–127

  14. 14.

    Ito K, Yanagimoto T, Iwata Y, Munehara H, Sakurai Y (2006) Genetic population structure of the spear squid Loligo bleekeri based on mitochondrial DNA. Nippon Suisan Gakkaishi 72:905–910 (In Japanese with English abstract)

  15. 15.

    Tomano S, Ahmad-Syazni K, Ueta Y, Ohara K, Umino T (2013) Eleven novel polymorphic microsatellite loci for oval squid Sepioteuthis lessoniana (Shiro-ika type). Int J Mol Sci 14:19971–19975

  16. 16.

    Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225. doi:10.3390/ijms141019971

  17. 17.

    Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis. Models and estimation procedures. Am J Hum Genet 19:233–257

  18. 18.

    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

  19. 19.

    Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581

  20. 20.

    Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

  21. 21.

    Hardy OJ, Charbonnel N, Fréville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482

  22. 22.

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

  23. 23.

    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

  24. 24.

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

  25. 25.

    Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572

  26. 26.

    Ueta Y, Segawa S (1995) Reproductive ecology and recruitment of juvenile of oval squid, Sepioteuthis lessoniana in outer waters adjacent to the Kii channel. Bull Jpn Soc Fish Oceangr 4:409–415 (In Japanese with English abstract)

  27. 27.

    Segawa S (1987) Life history of the oval squid, Sepioteuthis lessoniana in Kominato and adjacent waters central Honshu, Japan. J Tokyo Univ Fish 74:67–105

  28. 28.

    Sugimoto C, Ikeda Y (2012) Ontogeny of schooling behavior in the oval squid Sepioteuthis lessoniana. Fish Sci 78:287–294

  29. 29.

    Nabhitabhata J, Ikeda Y (2014) Chapter 17 Sepioteuthis lessonana. In: Culture Cephalopod (ed) Iglesias J, Fuentes L, Villanueva R. Springer, The Netherlands, pp 315–347

  30. 30.

    Shigeno S, Tsuchiya K, Segawa S (2001) Embryonic and paralarval development of the central nervous system of the loliginid squid Sepioteuthis lessoniana. J Comp Neurol 437:449–475

  31. 31.

    Dotsu K, Shima Y, Natsukari Y (1981) Ecology and fisheries of the oval squid, Sepioteuthis lessoniana Lesson in Goto Islands, Nagasaki prefecture. The Life of Goto Islands, Biol Soc Nagasaki Pref :457–465 (In Japanese)

  32. 32.

    Kanamaru H, Umeda T, Morikawa A (2007) Migration of the oval squid, Sepioteuthis lessoniana in northern and western waters of the Kyushu. Bull Saga Genkai Fish Res Dev Cent 4:51–57 (In Japanese)

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Acknowledgments

We gratefully acknowledge the assistance of people who helped with collecting specimens, Dr. Shiro Itoi (College of Bioresource Sciences, Nihon University), Mr. Atsushi Urabe (Kochi Prefectural Freshwater Fisheries Experimental Station), Dr. Akira Okamoto (Nagasaki Prefectural Government), Mr. Hiroyuki Hatanaka (Fukui Prefectural Fisheries Experimental Station), Ms. Shigemi Tsuda (Ishikawa Prefectural Fisheries Research Center), Mr. Kingo Tsumoto (Mie Prefectural Government), Mr. Kazuhiko Wada (Kagoshima Prefectural Government), and Mr. Makoto Watanabe (Miyazaki Prefectural Government). We would like to thank Dr. Tomoe Hikosaka for her cooperation and assistance in sequencing using the ABI 3130xl sequencer at the Gene Science Division, Natural Science Centre for Basic Research and Development, Hiroshima University. We also appreciate the cooperation of the executive committee of the squid fishing competition in Sukumo, Kochi Prefecture, and Breeden Co., Ltd., for kindly collecting specimens. This research was supported partly by Grants-in-Aid for Scientific Research (No. 26292106 for T.U.) from the Ministry of Education, Culture, Sport, Science, and Technology of Japan. This work was also supported by grants for a Research Fellowship from the Japan Society for Promotion of Science (JSPS) for Young Scientists to S.T.

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Correspondence to Tetsuya Umino.

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Tomano, S., Sanchez, G., Ueno, K. et al. Microsatellite DNA variation of oval squid Sepioteuthis sp. 2 reveals a single fishery stock on the coastline of mainland Japan. Fish Sci 81, 839–847 (2015). https://doi.org/10.1007/s12562-015-0905-4

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Keywords

  • Genetic diversity
  • Microsatellite loci
  • Oval squid
  • Sepioteuthis sp. 2
  • Population structure