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Genetic population structure and low genetic diversity in the over-exploited sea cucumber Holothuria edulis Lesson, 1830 (Echinodermata: Holothuroidea) in Okinawa Island

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Abstract

Understanding genetic connectivity is fundamental for ecosystem-based management of marine resources. Here we investigate the metapopulation structure of the edible sea cucumber Holothuria edulis Lesson, 1830 across Okinawa Island, Japan. This species is of economic and ecological importance and is distributed from the Red Sea to Hawai‘i. We examined sequence variation in fragments of mitochondrial cytochrome oxidase subunit I (COI) and 16S ribosomal RNA (16S), and nuclear histone (H3) at six locations across Okinawa Island. We found higher haplotype diversity for mtDNA (COI: Hd = 0.69 and 16S: Hd = 0.67) and higher heterozygosity of nDNA (H3: H E = 0.39) in populations from the west coast of Okinawa compared to individuals from populations on the east coast (COI: Hd = 0.40; 16S: Hd = 0.21; H3: H E = 0.14). Overall population structure was significant (AMOVA results for COI: Φ ST = 0.49, P < 0.0001; 16S: Φ ST = 0.34, P < 0.0001; H3: Φ ST = 0.12, P < 0.0001). One population in the east, Uruma, showed elevated pairwise Φ ST values in comparisons with all other sites and a marked reduction of genetic diversity (COI: Hd = 0.25 and 16S: Hd = 0.24), possibly as a consequence of a shift to a more dominant asexual reproduction mode. Recent reports have indicated that coastal development in this area influences many marine organisms, and ecosystem degradation in this location could cause the observed decrease of genetic diversity and isolation of H. edulis in Uruma. Our study should provide valuable data to help with the urgently needed management of sea cucumber populations in Okinawa, and indicates particular attention needs to be paid to vulnerable locations.

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Acknowledgments

The authors thank Dr. François Michonneau for providing technical advice during the DNA extraction and T. Ohara, O. Takama, K. Hamamoto, Dr. J. Montenegro, M. Mizuyama, and R. Diaz for help with sample collection. T.S. was supported by Ministry of Higher Education of the Egyptian Government during this study in Japan. J.D.R. was funded by a Japan Society for the Promotion of Science (JSPS) ‘Zuno-Junkan’ grant entitled ‘Studies on origin and maintenance of marine biodiversity and systematic conservation planning’. I.F.-S. was funded by a JSPS postdoctoral fellowship for overseas researchers. We thank two anonymous reviewers for their constructive comments, which improved the manuscript.

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Authors and Affiliations

  1. Molecular Invertebrate Systematics and Ecology Laboratory, Graduate School of Engineering and Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa, 903-0213, Japan

    Taha Soliman, Iria Fernandez-Silva & James Davis Reimer

  2. Aquaculture Department, National Institute of Oceanography and Fisheries, Kayet-Bay, El-Anfoushy, Alexandria, 21556, Egypt

    Taha Soliman

  3. Okinawa Institute of Science and Technology Graduate University, 1919-1 Tancha, Onna, Okinawa, 904-0495, Japan

    Taha Soliman

  4. Section of Ichthyology, California Academy of Sciences, 55 Music Concourse Dr., Golden Gate Park, San Francisco, CA, 94118, USA

    Iria Fernandez-Silva

  5. Department of Biochemistry, Genetics and Immunology, University of Vigo, Vigo, 36310, Spain

    Iria Fernandez-Silva

  6. Tropical Biosphere Research Center, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa, 903-0213, Japan

    James Davis Reimer

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  1. Taha Soliman
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Correspondence to Taha Soliman.

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10592_2016_823_MOESM1_ESM.ppt

Appendix S1. F ST pairwise values for Holothuria edulis across Okinawa Main Island inferred from mtDNA and nDNA. Sample sites are indicated in Table 1 and Fig. 1. Supplementary material 1 (PPT 196 kb)

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Soliman, T., Fernandez-Silva, I. & Reimer, J.D. Genetic population structure and low genetic diversity in the over-exploited sea cucumber Holothuria edulis Lesson, 1830 (Echinodermata: Holothuroidea) in Okinawa Island. Conserv Genet 17, 811–821 (2016). https://doi.org/10.1007/s10592-016-0823-8

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