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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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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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 | – | – | – | – | – | – | – | – |
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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