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Microsatellite Analysis of Japanese Sea Cucumber, Stichopus (Apostichopus) japonicus, Supports Reproductive Isolation in Color Variants

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Abstract

The genetic relationship among the three color variants (Red, Green, and Black) of the Japanese sea cucumber, S. japonicus, was investigated using 11 microsatellite markers. Genetic differentiation testing among the three sympatric color types showed the strong heterogeneity of Red (p < 0.001), while no significant difference was observed between Green and Black (p = 0.301 to 0.961). UPGMA trees constructed from 10 sample lots from 5 localities showed two distinct clusters, one from the Red types and the other from the Green and Black types. In addition, the sympatric Green and Black formed one subcluster with strong bootstrap support at each locality. These results indicate the separate species status of Red and the other color types, and also support the population identity of sympatric Green and Black.

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References

  • ME Arnegard JA Markert PD Danley JR Stauffer SuffixJr AJ Ambali TD Kocher (1999) ArticleTitlePopulation structure and colour variation of the cichlid fish Labeotropheus fuelleborni Ahl along a recently formed archipelago of rocky habitat patches in southern Lake Malawi Proc Roy Soc Lond B 266 119–130 Occurrence Handle10.1098/rspb.1999.0611

    Article  Google Scholar 

  • JFY Brookfield (1996) ArticleTitleA simple new method for estimating null allele frequency from heterozygote deficiency Mol Ecol 5 453–455 Occurrence Handle10.1046/j.1365-294X.1996.00098.x

    Article  Google Scholar 

  • S Choe Y Oshima (1961) ArticleTitleOn the morphological and ecological differences between two commercial forms, “Green” and “Red”, of the Japanese common sea cucumber, Stichopus japonicus SELENKA Nippon Suisan Gakkaishi 27 97–105

    Google Scholar 

  • D Dieringer C Schlötterer (2003) ArticleTitleMICROSATELLITE ANALYSER (MSA): a platform independent analysis tool for large microsatellite data sets Mol Ecol Notes 3 167–169 Occurrence Handle10.1046/j.1471-8286.2003.00351.x

    Article  Google Scholar 

  • A Mousadik ParticleEl RJ Petit (1996) ArticleTitleHigh level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco Theor Appl Genet 92 832–839 Occurrence Handle10.1007/s001220050200

    Article  Google Scholar 

  • KR Ewen M Bahlo SA Treloar DF Levinson B Mowry JW Barlow SJ Foote (2000) ArticleTitleIdentification and analysis of error types in high-throughput genotyping Am J Hum Genet 67 727–736 Occurrence Handle10.1086/303048

    Article  Google Scholar 

  • Felsenstein J (1993) PHYLIP (PHYLOGENY INFERENCE PACKAGE), version 3.5c. Department of Genetics, University of Washington, Seattle (program available from http://evolution.genetics. washington.edu/phylip.html)

  • DB Goldstein A Ruiz Linares LL Cavalli-Sforza MW Feldman (1995) ArticleTitleGenetic absolute dating based on microsatellites and the origin of modern humans Proc Natl Acad Sci USA 92 6723–6727 Occurrence Handle10.1073/pnas.92.15.6723

    Article  Google Scholar 

  • J Goudet (1995) ArticleTitleFSTAT (vers. 1.2): a computer program to calculate F-statistics J Hered 86 485–486

    Google Scholar 

  • OJ Hardy X Vekemans (2002) ArticleTitleSPAGeDi: a versatile computer program to analyze spatial genetic structure at the individual or population levels Mol Ecol Notes 2 618–620 Occurrence Handle10.1046/j.1471-8286.2002.00305.x

    Article  Google Scholar 

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

    Google Scholar 

  • AG Jones CA Stockwell D Walker JC Avise (1998) ArticleTitleThe molecular basis of a microsatellite null allele from the white sands pupfish J Hered 89 339–342 Occurrence Handle10.1093/jhered/89.4.339

    Article  Google Scholar 

  • M Kanno A Kijima (2001) ArticleTitleHigh genetic variability of isozymes in Japanese sea cucumber Stichopus japonicus Fish Genet Breed Sci 31 7–12

    Google Scholar 

  • M Kanno A Kijima (2002) ArticleTitleQuantitative and qualitative evaluation on the color variation of the Japanese sea cucumber Stichopus japonicus Suisan Zoshoku 50 63–69

    Google Scholar 

  • M Kanno A Kijima (2003) ArticleTitleGenetic differentiation among three color variants of Japanese sea cucumber Stichopus japonicus Fish Sci 69 806–812 Occurrence Handle10.1046/j.1444-2906.2003.00690.x

    Article  Google Scholar 

  • M Kanno Q Li A Kijima (2005) ArticleTitleIsolation and characterization of twenty microsatellite loci in the Japanese sea cucumber Stichopus japonicus Mar Biotechnol 7 179–183 Occurrence Handle10.1007/s10126-004-0006-3

    Article  Google Scholar 

  • Q Li C Park A Kijima (2003) ArticleTitleAllelic transmission of microsatellites and application to kinship analysis in newly hatched Pacific abalone larvae Fish Sci 69 881–887 Occurrence Handle10.1046/j.1444-2906.2003.00703.x

    Article  Google Scholar 

  • Q Li C Park T Kobayashi A Kijima (2003) ArticleTitleInheritance of microsatellite DNA markers in the Pacific abalone Haliotis discus hannai Mar Biotech 5 331–338 Occurrence Handle10.1007/s10126-002-0116-8

    Article  Google Scholar 

  • MA Mccartney K Brayer DR Levitan (2004) ArticleTitlePolymorphic microsatellite loci from the red urchin, Strongylocentrotus franciscanus, with comments on heterozygote deficit Mol Ecol Notes 4 226–228 Occurrence Handle10.1111/j.1471-8286.2004.00624.x

    Article  Google Scholar 

  • M Nei (1978) ArticleTitleEstimation of average heterozygosity and genetic distance from a number of individuals Genetics 89 538–590

    Google Scholar 

  • CV Oosterhout WF Hutchinson DPM Wills P Shipley (2004) ArticleTitleMICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data Mol Ecol Notes 4 535–538 Occurrence Handle10.1111/j.1471-8286.2004.00684.x

    Article  Google Scholar 

  • M Raymond F Rousset (1995) ArticleTitleGENEPOP (version1.2): population genetics software for exact tests and ecumenicism J Hered 86 248–249

    Google Scholar 

  • M Raymond F Rousset (1995) ArticleTitleAn exact test for population differentiation Evolution 49 1280–1283 Occurrence Handle10.2307/2410454

    Article  Google Scholar 

  • C Schlötterer (2001) ArticleTitleGenealogical inference of closely related species based on microsatellites Genet Res Camb 78 209–212

    Google Scholar 

  • M Slatkin (1995) ArticleTitleA measure of population subdivision based on microsatellite allele frequencies Genetics 139 457–462

    Google Scholar 

  • T Sugaya M Ikeda H Mori N Taniguchi (2002) ArticleTitleInheritance mode of microsatellite DNA markers and their use for kinship estimation in kuruma prawn Penaeus japonicus Fish Sci 68 299–305 Occurrence Handle10.1046/j.1444-2906.2002.00425.x

    Article  Google Scholar 

  • MJH Oppen ParticleVan GF Turner CRRL Robinson JC Deutsch MJ Genner GM Hewitt (1998) ArticleTitleAssortative mating among rock-dwelling cichlid fishes supports high estimates of species richness from Lake Malawi Mol Ecol 7 991–1001 Occurrence Handle10.1046/j.1365-294x.1998.00417.x

    Article  Google Scholar 

  • JM Waters YB Esa GP Wallis (2001) ArticleTitleGenetic and morphological evidence for reproductive isolations of Galaxias (Teoleostei: Galaxiidae) in South Island, New Zealand Biol J Linn Soc 73 287–298 Occurrence Handle10.1006/bijl.2001.0541

    Article  Google Scholar 

  • R Wattier CR Engel P Saumitou-Laprade M Valero (1998) ArticleTitleShort allele dominance as a source of heterozygote deficiency at microsatellite loci: experimental evidence at the dinucleotide locus Gv1CT in Gracilaria gracilis (Rhodophyta) Mol Ecol 7 1569–1573 Occurrence Handle10.1046/j.1365-294x.1998.00477.x

    Article  Google Scholar 

  • BS Weir CC Cockerham (1984) ArticleTitleEstimating F-statistics for the analysis of population structure Evolution 38 1358–1370 Occurrence Handle10.2307/2408641

    Article  Google Scholar 

  • K Yamamoto T Handa K Fujimoto (2003) ArticleTitleDifferences in tolerance to low-salinity among red, blue and black (color pattegrn) of the Japanese common sea cucumber, Apostichopus japonicus from ventilation in the respiratory tree SUISANZOSHOKU 51 321–326

    Google Scholar 

  • K Yamamoto T Handa K Fujimoto (2005) ArticleTitleEffect of water temperature on ventilation of the Japanese common sea cucumber, Apostichopus japonicus of different color pattern SUISAN ZOSHOKU 53 67–74

    Google Scholar 

Download references

Acknowledgments

The authors thank Professor Hiroyuki Munehara of Hokkaido University, Dr. Yoshinobu Kosaka of Aomori Prefectural Aquaculture Research Center, and Mr. Yoshihiro Yamamoto of Oita Institute of Marine and Fisheries Science for collecting samples. This study was supported in part by the Grant-in-Aid for Scientific Research (No. 13460080) from the Japanese Ministry of Education, Culture, Sports, Science and Technology.

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Correspondence to Akihiro Kijima.

Appendix

Appendix

Allele Frequencies of 11 Microsatellite Loci on Each Sample Lot

Locus

Allele

Miyagi

Oita

Aomori

Hokkaido

Qingdao

Red

Green

Black

Red

Green

Black

Green

Black

Green

Green

Psj1828

(n)

(53)

(50)

(50)

(37)

(42)

(27)

(30)

(29)

(32)

(41)

171

0.012

174

0.047

0.010

0.010

0.041

176

0.038

0.060

0.060

0.054

0.036

0.019

0.033

0.024

178

0.047

0.010

0.030

0.108

0.095

0.074

0.033

0.034

0.061

179

0.010

0.024

0.017

0.016

0.012

180

0.009

0.010

182

0.443

0.250

0.240

0.514

0.321

0.389

0.367

0.259

0.312

0.378

183

0.179

0.010

0.030

0.122

0.012

0.017

0.017

184

0.010

0.010

0.027

186

0.009

0.020

0.027

0.019

0.017

192

0.009

0.190

0.150

0.133

0.190

0.188

0.049

194

0.094

0.060

0.040

0.068

0.119

0.037

0.150

0.103

0.125

0.098

196

0.075

0.050

0.027

0.031

198

0.038

0.260

0.280

0.345

0.389

0.200

0.310

0.312

0.341

200

0.030

0.060

0.014

0.012

0.056

0.017

202

0.009

0.040

0.060

0.036

0.019

0.033

0.052

0.016

0.024

204

0.010

206

0.017

Psj2031

(n)

(53)

(47)

(50)

(38)

(42)

(27)

(30)

(28)

(30)

(41)

178

0.013

179

0.028

0.039

180

0.028

181

0.017

182

0.010

0.017

0.018

183

0.011

0.018

0.017

184

0.009

0.011

0.013

0.036

185

0.038

0.010

0.066

0.012

186

0.028

0.011

0.020

0.013

0.036

0.037

0.017

0.036

0.017

0.012

187

0.113

0.043

0.010

0.092

0.024

0.019

0.017

0.033

0.037

188

0.038

0.085

0.080

0.092

0.095

0.074

0.033

0.054

0.050

0.134

189

0.453

0.117

0.050

0.513

0.143

0.093

0.017

0.107

0.050

0.037

190

0.179

0.043

0.140

0.039

0.083

0.019

0.200

0.071

0.083

0.085

191

0.009

0.117

0.090

0.053

0.048

0.056

0.050

0.036

0.033

0.049

192

0.043

0.090

0.107

0.111

0.100

0.125

0.033

0.085

193

0.009

0.053

0.080

0.026

0.012

0.037

0.117

0.089

0.133

0.146

194

0.128

0.070

0.024

0.019

0.050

0.125

0.133

0.146

195

0.047

0.074

0.090

0.039

0.083

0.093

0.050

0.085

196

0.021

0.040

0.012

0.056

0.067

0.071

0.033

0.024

197

0.021

0.010

0.071

0.093

0.083

0.017

0.049

198

0.011

0.020

0.024

0.019

0.017

0.036

0.033

199

0.021

0.024

0.019

0.017

0.071

0.083

200

0.019

0.032

0.060

0.012

0.019

0.033

0.018

0.117

0.024

201

0.032

0.030

0.024

0.019

0.017

0.018

0.033

0.037

202

0.064

0.050

0.036

0.074

0.017

0.054

0.050

0.012

203

0.011

0.010

0.036

0.074

0.017

0.017

204

0.011

0.010

0.017

205

0.011

0.010

0.012

0.019

0.017

0.017

0.012

206

0.011

0.012

207

0.010

0.024

0.024

208

0.012

0.019

209

0.011

0.012

0.037

210

0.024

0.017

0.018

212

0.010

215

0.011

220

0.017

Psj2172

(n)

(54)

(51)

(50)

(38)

(41)

(24)

(30)

(29)

(32)

(39)

164

0.017

167

0.602

0.137

0.110

0.500

0.098

0.104

0.167

0.086

0.078

0.154

169

0.102

0.010

0.237

0.012

0.017

171

0.222

0.029

0.010

0.250

0.042

0.017

173

0.009

0.013

0.024

174

0.046

0.676

0.760

0.610

0.729

0.550

0.655

0.797

0.744

175

0.009

176

0.009

0.039

0.010

0.024

0.017

0.013

178

0.010

0.049

0.021

0.034

0.038

179

0.108

0.100

0.183

0.104

0.233

0.207

0.125

0.051

Psj2368

(n)

(54)

(49)

(50)

(38)

(39)

(26)

(29)

(29)

(33)

(39)

195

0.222

0.010

0.010

0.158

0.058

0.052

0.038

196

0.019

197

0.037

0.039

199

0.111

0.010

0.118

0.026

200

0.157

0.031

0.030

0.132

0.017

0.017

0.013

201

0.222

0.061

0.090

0.395

0.205

0.115

0.155

0.224

0.121

0.141

202

0.074

0.102

0.120

0.039

0.051

0.115

0.121

0.069

0.106

0.154

203

0.009

0.020

0.019

204

0.019

0.143

0.040

0.051

0.038

0.224

0.241

0.076

0.064

205

0.065

0.031

0.066

0.017

0.017

0.015

0.013

206

0.028

0.010

0.060

0.026

0.034

0.069

0.076

0.026

207

0.037

0.490

0.580

0.026

0.526

0.538

0.362

0.190

0.530

0.526

208

0.092

0.040

0.167

0.115

0.052

0.086

0.045

209

0.017

0.015

210

0.010

0.017

0.015

211

0.020

0.017

Psj2463

(n)

(53)

(53)

(53)

(38)

(42)

(27)

(29)

(29)

(34)

(41)

233

0.009

0.026

234

0.925

0.075

0.038

0.921

0.024

0.056

0.029

236

0.009

0.009

0.039

238

0.013

241

0.292

0.358

0.048

0.074

0.345

0.276

0.397

0.195

243

0.009

0.085

0.104

0.012

0.017

0.121

0.162

0.012

244

0.028

0.015

245

0.015

0.024

249

0.009

0.009

0.071

0.037

0.044

0.012

251

0.015

252

0.009

0.028

0.047

0.052

0.069

0.088

253

0.019

0.012

0.056

0.024

254

0.009

0.012

255

0.028

0.358

0.377

0.667

0.704

0.483

0.466

0.221

0.598

257

0.012

0.017

259

0.066

0.028

0.060

0.037

0.069

0.017

0.015

0.098

260

0.012

261

0.009

0.038

0.009

0.083

0.037

0.034

0.034

0.012

265

0.009

271

0.012

Psj2575

(n)

(53)

(54)

(54)

(36)

(42)

(27)

(30)

(29)

(34)

(41)

89

0.028

0.009

0.042

0.017

0.024

91

0.198

0.120

0.157

0.208

0.095

0.093

0.083

0.190

0.265

0.171

93

0.340

0.130

0.204

0.361

0.119

0.167

0.183

0.155

0.132

0.171

95

0.292

0.648

0.556

0.319

0.726

0.722

0.617

0.534

0.471

0.500

97

0.075

0.028

0.046

0.028

0.050

0.034

0.103

0.073

99

0.066

0.028

0.019

0.042

0.024

0.019

0.067

0.017

0.029

0.037

100

0.009

101

0.009

0.012

103

0.009

0.012

0.034

105

0.009

0.009

0.012

107

0.009

0.012

0.017

0.012

Psj2844

(n)

(53)

(53)

(52)

(37)

(42)

(27)

(30)

(29)

(32)

(41)

158

0.019

0.019

0.014

160

0.019

0.009

0.029

0.014

0.017

0.016

162

0.934

0.906

0.856

0.919

0.988

0.963

0.933

0.948

0.844

0.878

164

0.028

0.075

0.077

0.054

0.012

0.037

0.067

0.034

0.141

0.122

167

0.009

0.019

Psj2889

(n)

(54)

(53)

(48)

(37)

(41)

(27)

(30)

(29)

(32)

(40)

194

0.009

0.010

204

0.398

0.047

0.052

0.500

0.012

0.037

0.031

0.013

206

0.019

0.010

0.031

0.013

207

0.009

208

0.472

0.038

0.010

0.419

0.012

0.017

0.031

210

0.019

0.010

0.050

0.034

0.109

212

0.028

0.009

0.031

0.014

0.049

0.056

0.033

0.034

0.075

214

0.009

0.066

0.073

0.014

0.110

0.130

0.083

0.052

0.125

0.175

216

0.028

0.019

0.031

0.054

0.037

0.056

0.017

0.031

0.087

218

0.009

0.104

0.198

0.220

0.148

0.100

0.172

0.125

0.112

220

0.019

0.283

0.177

0.122

0.093

0.200

0.207

0.188

0.138

222

0.217

0.156

0.207

0.259

0.217

0.241

0.109

0.150

223

0.009

0.010

0.019

224

0.160

0.135

0.122

0.093

0.200

0.190

0.188

0.150

226

0.009

0.073

0.073

0.037

0.067

0.034

0.016

0.038

228

0.009

0.010

0.012

0.019

0.016

0.038

230

0.009

0.013

232

0.033

0.017

234

0.010

0.024

0.056

Psj2969

(n)

(52)

(53)

(53)

(37)

(42)

(27)

(30)

(29)

(33)

(40)

130

0.014

0.017

132

0.019

0.017

134

0.019

0.047

0.075

0.012

0.019

0.050

0.052

0.091

0.087

136

0.731

0.057

0.075

0.905

0.083

0.056

0.050

0.052

0.045

0.075

138

0.125

0.311

0.387

0.041

0.274

0.333

0.200

0.207

0.470

0.287

140

0.058

0.245

0.245

0.027

0.321

0.222

0.383

0.328

0.167

0.225

142

0.067

0.274

0.189

0.014

0.298

0.370

0.267

0.259

0.212

0.300

144

0.009

0.019

0.012

146

0.013

150

0.019

0.009

0.033

0.086

0.015

0.013

152

0.019

Psj3072

(n)

(52)

(51)

(54)

(38)

(42)

(27)

(30)

(29)

(29)

(40)

159

0.013

161

0.010

0.066

0.019

162

0.010

0.010

0.009

0.017

0.052

163

0.049

0.037

0.013

0.024

0.037

0.050

0.017

0.017

164

0.038

0.019

0.066

0.050

0.034

165

0.019

0.010

0.009

0.039

0.017

0.062

166

0.019

0.013

0.012

0.034

0.038

167

0.038

0.019

0.013

0.017

0.017

0.034

0.025

168

0.019

0.013

0.024

0.037

169

0.010

0.036

0.019

0.017

0.034

170

0.010

0.284

0.389

0.026

0.417

0.426

0.483

0.397

0.328

0.325

171

0.012

0.013

172

0.010

0.020

0.019

0.036

0.074

0.034

0.017

173

0.038

0.186

0.120

0.013

0.155

0.130

0.217

0.190

0.224

0.237

174

0.010

0.010

0.009

0.036

0.037

0.017

0.017

175

0.067

0.010

0.037

0.066

0.017

0.069

0.052

0.025

176

0.010

0.009

0.012

177

0.067

0.049

0.065

0.092

0.012

0.034

0.034

0.050

179

0.202

0.029

0.009

0.197

0.036

0.056

0.083

0.052

0.069

0.050

180

0.019

0.010

0.009

0.017

181

0.154

0.069

0.028

0.184

0.060

0.056

0.017

0.052

0.062

182

0.013

183

0.048

0.029

0.009

0.026

0.060

0.074

0.017

0.017

184

0.049

0.056

0.017

0.025

185

0.163

0.069

0.037

0.105

0.024

0.019

0.017

187

0.048

0.010

0.056

0.039

0.017

0.017

0.013

189

0.019

0.049

0.028

0.013

0.036

0.019

0.034

0.050

191

0.020

0.017

193

0.010

0.010

0.013

0.012

0.017

195

0.010

0.009

Psj3088

(n)

(54)

(54)

(54)

(34)

(42)

(27)

(30)

(29)

(31)

(41)

161

0.017

163

0.012

165

0.028

0.102

0.139

0.015

0.155

0.222

0.200

0.224

0.065

0.146

168

0.019

0.009

0.074

0.012

169

0.009

0.019

0.015

0.024

0.017

170

0.093

0.028

0.028

0.074

0.033

0.017

171

0.287

0.759

0.750

0.221

0.738

0.685

0.683

0.690

0.887

0.817

172

0.574

0.093

0.056

0.603

0.071

0.093

0.083

0.034

0.016

0.024

175

0.016

177

0.016

183

0.009

  1. (n) : number of samples.

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Kanno, M., Suyama, Y., Li, Q. et al. Microsatellite Analysis of Japanese Sea Cucumber, Stichopus (Apostichopus) japonicus, Supports Reproductive Isolation in Color Variants. Mar Biotechnol 8, 672–685 (2006). https://doi.org/10.1007/s10126-006-6014-8

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  • DOI: https://doi.org/10.1007/s10126-006-6014-8

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