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Conservation Genetics

, Volume 17, Issue 4, pp 811–821 | Cite as

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

  • Taha Soliman
  • Iria Fernandez-Silva
  • James Davis Reimer
Research Article

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.

Keywords

Genetic diversity Coastal development Genetic structure mtDNA Okinawa Sea cucumber 

Notes

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.

Supplementary material

10592_2016_823_MOESM1_ESM.ppt (196 kb)
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)

References

  1. Acker JG, Leptoukh G (2007) Online analysis enhances use of NASA earth science data. EOS Trans Am Geophys Union 88(2):14–17CrossRefGoogle Scholar
  2. Arndt A, Marquez C, Lambert P, Smith MJ (1996) Molecular phylogeny of eastern Pacific sea cucumbers (Echinodermata: Holothuroidea) based on mitochondrial DNA sequence. Mol Phylogenet Evol 6:425–437CrossRefPubMedGoogle Scholar
  3. Bandelt H, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48CrossRefPubMedGoogle Scholar
  4. Borrero-Pérez G, González-Wangüemert M, Pérez-Ruzafa A, Marcos C (2011) Phylogeography of the Atlanto-Mediterranean sea cucumber Holothuria (Holothuria) mammata: the combined effects of historical processes and current oceanographical pattern. Mol Ecol 20:1964–1975CrossRefPubMedGoogle Scholar
  5. Castelin M, Lorion J, Brisset J, Cruaud C, Maestrati P, Utge J, Samadi S (2012) Speciation patterns in gastropods with long-lived larvae from deep-sea seamounts. Mol Ecol 21:4828–4853CrossRefPubMedGoogle Scholar
  6. Choo PS (2008) Population status, fisheries and trade of sea cucumbers in Asia. In: M.V. Toral-Granda, A. Lovatelli, M. Vasconcellos. (ed.), Sea cucumbers. A global review on fisheries and trade. FAO, RomeGoogle Scholar
  7. Colgan DJ, McLauchlan A, Wilson GDF, Livingston S, Macaranas J, Edgecombe GD, Cassis G, Gray MR (1998) Molecular phylogenetics of the Arthropoda: relationships based on histone H3 and U2 snRNA DNA sequences. Aust J Zool 46:419–437CrossRefGoogle Scholar
  8. Conand C (1996) Asexual reproduction by fission in Holothuria atra: variability of some parameters in populations from the tropical Indo-Pacific. Oceanol Acta 19(3–4):209–216Google Scholar
  9. Conand C (2008) Population status, fisheries and trade of sea cucumbers in Africa and Indian Ocean, In Toral-Granda V., Lovatelli A. and Vasconcellos M. (eds). Sea cucumbers. A global review on fishery and trade. FAO Fisheries Technical Paper No. 516. FAO, Rome, pp 153–205Google Scholar
  10. Conand C, Muthiga N. (eds) (2007) Commercial sea cucumbers: a review for the Western Indian Ocean. WIOMSA Book Series No. 5Google Scholar
  11. Conroy CJ, Cook JA (2000) Phylogeography of a post-glacial colonizer: Microtus longicaudus (Rodentia: Muridae). Mol Ecol 9:165–175CrossRefPubMedGoogle Scholar
  12. Dissanayake DCT, Stefansson G (2010) Abundance and distribution of commercial sea cucumbers in the coastal waters of Sri Lanka. Aquat Living Resour 23(3):303–313CrossRefGoogle Scholar
  13. 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 Resour 10:564–567CrossRefPubMedGoogle Scholar
  14. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  15. Friedman K, Eriksson H, Tardy E, Pakoa K (2011) Management of sea cucumber stocks: patterns of vulnerability and recovery of sea cucumber stocks impacted by fishing. Fish Fish 12:75–93CrossRefGoogle Scholar
  16. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentralGoogle Scholar
  17. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6:13. v.3.23 http://ibdws.sdsu.edu/
  18. Kamidaira Y, Uchiyama Y, Mitarai S, Sakagami T (2014) Effects of the submesoscale anticyclonic eddies induced by Kuroshio in East China Sea. Proceedings of the Twenty-fourth International Ocean and Polar Engineering Conference Busan, Korea, June 15–20Google Scholar
  19. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  20. Laxminarayana A (2005) Induced spawning and larval rearing of the sea cucumbers, Bohadschia marmorata and Holothuria atra in Mauritius. SPC Beche-de-mer Inf Bull 22:48–52Google Scholar
  21. Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55:955–975CrossRefPubMedGoogle Scholar
  22. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  23. Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787CrossRefGoogle Scholar
  24. Ni G, Li Q, Kong L, Yu H (2014) Comparative phylogeography in marginal seas of the northwestern Pacific. Mol Ecol 23:534–548CrossRefPubMedGoogle Scholar
  25. Palumbi SR, Martin AP, Romano S, Mcmilla WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. Department of Zoology, University of Hawai‘i, HonoluluGoogle Scholar
  26. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  27. Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mills LS, Gretchen D, Castilla JC, Lubchenco J, Paine RT (1996) Challenges in the quest for keystones. Bioscience 46:609–620CrossRefGoogle Scholar
  28. Purcell SW, Gossuin H, Agudo NS (2009) Status and management of the sea cucumber fishery of La Grande Terre, New Caledonia. WorldFish Center Studies and Reviews. Penang, Malaysia: The WorldFish CenterGoogle Scholar
  29. Purcell SW, Lovatelli A, Pakoa K (2014a) Constraints and solutions for managing Pacific Island sea cucumber fisheries with an ecosystem approach. Mar Policy 45:240–250CrossRefGoogle Scholar
  30. Purcell SW, Polidoro BA, Hamel J-F, Gamboa RU, Mercier A (2014b) The cost of being valuable: predictors of extinction risk in marine invertebrates exploited as luxury seafood. Proc R Soc 281:2013–3296Google Scholar
  31. Reimer JD, Yang S-Y, White KN, Asami R, Fujita K, Hongo C, Ito S, Kawamura I, Maeda B, Mizuyama M, Obuchi M, Sakamaki T, Tachihara K, Tamura K, Tanahara A, Yamaguchi A, Jenke-Kodama H (2015) Effects of causeway construction on environment and biota of subtropical tidal flats in Okinawa, Japan. Mar Pollut Bull 94(1–2):153–167CrossRefPubMedGoogle Scholar
  32. Rodrigues F, Valente S, González-Wangüemert M (2015) Genetic diversity across geographical scales in marine coastal ecosystems: Holothuria arguinensis a model species. J Exp Mar Biol Ecol 463:158–167CrossRefGoogle Scholar
  33. Schneider K, Silverman J, Woolsey E, Eriksson H, Byrne M, Caldeira K (2011) Potential influence of sea cucumbers on coral reef CaCO3 budget: a case study at One Tree Reef. J Geophys Res 116:G04032CrossRefGoogle Scholar
  34. Skillings DJ, Bird CE, Toonen RJ (2014) Comparative population structure of two edible Indo-Pacific coral reef sea cucumbers (Echinodermata: Holothuroidea). Bull Mar Sci 90(1):359–378CrossRefGoogle Scholar
  35. Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169CrossRefPubMedPubMedCentralGoogle Scholar
  36. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  37. Toonen RJ, Andrews KR, Baums IB, Bird CE, Concepcion CT, Daly-Engel TS, Eble JA, Faucci A, Gaither MR, Iacchei M, Puritz JB, Schultz JK, Skillings DJ, Timmers MA Bowen BW (2011) Defining boundaries for applying ecosystem-based management: a multispecies case study of marine connectivity across the Hawaiian Archipelago. J Mar Biol #460173Google Scholar
  38. Toral-Granda V (2008) Galapagos Islands: a hotspot of sea cucumber fisheries in Central and South America. In V. Toral-Granda, A. Lovatelli and M. Vasconcellos (eds). Sea cucumbers. A global review of fisheries and trade. FAO Fisheries and Aquaculture Technical Paper. No. 516. Rome, FAO, pp 231–253Google Scholar
  39. Uthicke S (1997) The seasonality of asexual reproduction in Holothuria (Halodeima) atra, Holothuria (Halodeima) edulis and Stichopus chloronotus (Holothuroidea: Aspidochirotida) on the Great Barrier Reef. Mar Biol 129:435–441CrossRefGoogle Scholar
  40. Uthicke S, Schaffelke B, Byrne M (2009) A boom–bust phylum? Ecological and evolutionary consequences of density variations in echinoderms. Ecol Monogr 79:3–24CrossRefGoogle Scholar
  41. Valente S, Serrão EA, González-Wangüemert M (2014) West versus East Mediterranean Sea: origin and genetic differentiation of the sea cucumber Holothuria polii. Mar Ecol. doi: 10.1111/maec.12156 Google Scholar
  42. Vergara-Chen C, González-Wangüemert M, Marcos C, Perez-Ruzafa A (2010) Genetic diversity and connectivity remain high in Holothuria polii (Delle Chiaje 1823) across a coastal lagoon-open sea environmental gradient. Genetica 138:895–906CrossRefPubMedGoogle Scholar
  43. Weir BS, Cockerham CC (1984) Estimating F–statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  44. White KN, Lorion J, Reimer JD (2015) Preliminary analyses reveal strong genetic structure in populations of Leucothoe vulgaris (Crustacea: Amphipoda: Leucothoidae) from Okinawa Japan. Syst Biodivers. doi: 10.1080/14772000.2015.1078856 Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Taha Soliman
    • 1
    • 2
    • 3
  • Iria Fernandez-Silva
    • 1
    • 4
    • 5
  • James Davis Reimer
    • 1
    • 6
  1. 1.Molecular Invertebrate Systematics and Ecology Laboratory, Graduate School of Engineering and ScienceUniversity of the RyukyusOkinawaJapan
  2. 2.Aquaculture DepartmentNational Institute of Oceanography and FisheriesAlexandriaEgypt
  3. 3.Okinawa Institute of Science and Technology Graduate UniversityOkinawaJapan
  4. 4.Section of IchthyologyCalifornia Academy of SciencesSan FranciscoUSA
  5. 5.Department of Biochemistry, Genetics and ImmunologyUniversity of VigoVigoSpain
  6. 6.Tropical Biosphere Research CenterUniversity of the RyukyusOkinawaJapan

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