Abstract The genetic structure of the populations of the sword prawn Parapenaeopsis hardwickii (Miers, 1878) in the Yellow Sea and East China Sea, an economically and ecologically important species in the Indo-West Pacific region, is described. Based on partial mtDNA COI gene, 27 COI haplotypes are recognized from 130 samples collected from seven locations. Nucleotide and haplotype diversities of the Yellow Sea and East China Sea populations were 0.00187 ± 0.00021 and 0.818 ± 0.049, and 0.00215 ± 0.00023 and 0.822 ± 0.042, respectively. AMOVA and pairwise FST reveal no significant genetic differentiation of the populations. Neither the Bayesian inference tree nor haplotype network reveals clades with geographic pattern, indicating high levels of gene flow between prawn populations of each sea. Mismatch distribution and neutrality tests suggest an historical population expansion of P. hardwickii, with Pleistocene glacial cycles likely having impacted this species’ historical demography. This study provides background information for sustainable improvement and fisheries management of P. hardwickii in the Yellow Sea and East China Sea. INTRODUCTION Given high dispersal potential of planktonic egg, larval, and adult life-history stages, and a lack of obvious physical barriers to gene flow in the open sea, marine organisms generally show low levels of genetic differentiation over large geographic scales (Grant & Bowen, 1998; Avise, 2000; Hewitt, 2000). Mounting evidence nevertheless reveals distinct genetic patterns in some sympatric taxa, with some species having, yet others lacking, significant population divergence (Shen et al., 2011; Ni et al., 2012; Alam et al., 2016, 2017). Restrictions vary widely among species, their life histories, habitats, historical events and hydrological factors, all of which potentially influence genetic differentiation (Palumbi, 1994; Ni et al., 2014). The marginal seas of China are among the most extensive in the western Pacific. Their oceanography and dramatic geological history are well characterized. Accordingly, these waters provide a model environment in which to study the genetics and phylogeography of the populations of marine organisms (Kong & Li, 2009). Research on mollusk, crustacean, and fish taxa has revealed how the separation and coastal topography, ocean currents, and freshwater outflow of the Pleistocene glacial sea basin have influenced the genetic structure of species (Liu et al., 2007; Shen et al., 2011; Dong et al., 2012; Ni et al., 2014). The ecologically and economically important sword prawn Parapenaeopsis hardwickii (Miers, 1878) (Decapoda: Penaeidae) occurs in the Indo-West Pacific from Pakistan to Japan (Song & Ding, 1993). During spring and summer this species typically resides in coastal waters from 5–70 m, but moves to deeper water in cooler seasons (Wei, 1991). Although its fishery is one of the most valuable in China, East China Sea stocks fell almost three-quarters from the mid-1980s to 1998 (Song et al., 2009). Wild-stock declines of this magnitude inevitably reduced intraspecific genetic diversity, and led to losses of germplasm resources. Despite this, most research on P. hardwickii has focused on its fisheries biology and artificial breeding (Song et al., 2009; Zhang et al., 2011; Liu et al., 2013), leading to limited genetic information being available (Tzeng et al., 2007, 2008). Given stable maternal inheritance, lack of recombination, and rapid evolutionary rate, mitochondrial DNA (mtDNA) markers have been widely used in studies of intraspecific population genetics (De Bruyn et al., 2005; Alam et al., 2015). We report genetic diversity and population genetic structure of P. hardwickii from the Yellow Sea and East China Sea using mtDNA cytochrome c oxidase subunit I (COI) sequence data. This information is important for sustainable and effective fishery management. MATERIALS AND METHODS Sampling Sword prawns (130) were collected from seven locations (13–24 individuals per location) in the Yellow Sea and East China Sea (Fig. 1, Table 1) between June 2014 and November 2015. Samples identities were confirmed with the morphological features, and then preserved in 95% ethanol for DNA extraction. Figure 1. View largeDownload slide Sampling locations of Parapenaeopsis hardwickii in the Yellow Sea (Y1-Y3) and East China Sea (E1-E4). The arrows illustrate the currents (operating in summer, from Su & Yuan, 2005) in the studied area. Currents: SBCC, Subei Coastal Current; CCC, China Coastal Current; CDW, Changjiang diluted water; KC, Kuroshio Current; TC, Tsushima Current. Figure 1. View largeDownload slide Sampling locations of Parapenaeopsis hardwickii in the Yellow Sea (Y1-Y3) and East China Sea (E1-E4). The arrows illustrate the currents (operating in summer, from Su & Yuan, 2005) in the studied area. Currents: SBCC, Subei Coastal Current; CCC, China Coastal Current; CDW, Changjiang diluted water; KC, Kuroshio Current; TC, Tsushima Current. Table 1. Sampling information and genetic diversity index of Parapenaeopsis hardwickii from the Yellow Sea and East China Sea. Biogeographic region Population (Locality) Sample size Number of haplotypes Nucleotide diversity (π) Haplotype diversity (h) Yellow Sea Y1 (35.0°N, 124.0°E) 17 7 0.00167 ± 0.00036 0.772 ± 0.096 Y2 (33.0°N, 121.6°E) 24 10 0.00202 ± 0.00032 0.848 ± 0.063 Y3 (32.5°N, 123.0°E) 19 9 0.00183 ± 0.00035 0.819 ± 0.082 East China Sea E1 (30.0°N, 122.5°E) 22 12 0.00199 ± 0.00036 0.835 ± 0.077 E2 (29.0°N, 122.4°E) 20 10 0.00201 ± 0.00036 0.837 ± 0.076 E3 (27.8°N, 121.9°E) 15 7 0.00204 ± 0.00047 0.829 ± 0.082 E4 (26.8°N, 120.8°E) 13 7 0.00278 ± 0.00064 0.846 ± 0.085 Total 130 27 0.00202 ± 0.00016 0.818 ± 0.032 Biogeographic region Population (Locality) Sample size Number of haplotypes Nucleotide diversity (π) Haplotype diversity (h) Yellow Sea Y1 (35.0°N, 124.0°E) 17 7 0.00167 ± 0.00036 0.772 ± 0.096 Y2 (33.0°N, 121.6°E) 24 10 0.00202 ± 0.00032 0.848 ± 0.063 Y3 (32.5°N, 123.0°E) 19 9 0.00183 ± 0.00035 0.819 ± 0.082 East China Sea E1 (30.0°N, 122.5°E) 22 12 0.00199 ± 0.00036 0.835 ± 0.077 E2 (29.0°N, 122.4°E) 20 10 0.00201 ± 0.00036 0.837 ± 0.076 E3 (27.8°N, 121.9°E) 15 7 0.00204 ± 0.00047 0.829 ± 0.082 E4 (26.8°N, 120.8°E) 13 7 0.00278 ± 0.00064 0.846 ± 0.085 Total 130 27 0.00202 ± 0.00016 0.818 ± 0.032 View Large DNA extraction, amplification, and sequencing Genomic DNA was extracted from muscle tissue using a Tissue DNA Kit (Omega Bio-Tech, Norcross, GA, USA). For each individual, fragments of mtDNA COI gene were amplified with universal primer pairs: LCO 1490 (5′- GGTCAACAAATCATAAAGATATTGG-3′), and HCO 2198 (5′- TAAACTTCAGGGTGAC CAAAAAATCA-3′) (Folmer et al., 1994). PCR amplifications were carried out in a 30 μl volume containing 2 units Taq DNA polymerase (TaKaRa, Dalian, China), 100 ng template DNA, 200 nM/l forward and reverse primers, 200 mM/l of each dNTPs, 10 mM/l Tris (pH 8.3), 50 mM/l KCl, and 1.5 mM/l MgCl2. Cycling conditions entailed initial denaturation at 94 ºC for 3 min, followed by 40 cycles of 94 ºC for 45 s, 50 ºC for 30 s, and 72 ºC for 45 s, followed by a final extension at 72 ºC for 10 min. PCR products were purified using the PCR clean-up Kit (Axygen, New York, NY, USA) and sequenced using an ABI 3730 automatic sequencer (Sangon, Dalian, China). Analyses of data Sequences were assembled and edited by DNASTAR and aligned with Clustal X (Thompson et al., 1997). Homology analysis of sequences was done through BLASTN in NCBI. And the accuracy of COI sequences was further confirmed by translating the nucleotide data to amino acid sequences. Nucleotide (π) and haplotype (h) diversities were calculated using the DnaSP (Librado & Rozas, 2009). Phylogenetic relationships among haplotypes were reconstructed using Bayesian inference (BI) in MrBayes 3.2.6 (Ronquist & Huelsenbeck, 2003); the HKY model was selected using Modeltest (Posada, 2008). Four Markov chains run for 106 generations were sampled every 100 generations to yield a posterior probability distribution of 104 trees; the first 2500 trees were discarded as burn-in. A median-joining (MJ) network was generated for all haplotypes using the program Network 220.127.116.11 (Bandelt et al., 1999). Population genetic structure was evaluated with analysis of molecular variance (AMOVA) (Excoffier et al., 1992) and FST statistics in ARLEQUIN (Excoffier & Lischer, 2010). Historical demographic changes in P. hardwickii were examined using Tajima’s D (Tajima, 1989) statistics and Fu’s Fs (Fu, 1997) test, to determine if neutrality held. Negative values of Tajima’s D and Fu’s Fs were considered to represent population expansion, whereas positive values suggested either balancing selection or secondary contact among previously isolated lineages. The frequency distribution of pairwise differences between mtDNA haplotypes (i.e., mismatch distribution) was used to infer historic demographic expansions. If a rapid expansion was observed in demographic analysis, the formula t = τ/(2 μk) (Rogers & Harpending, 1992) was used to further estimate time of expansion, in which tau (τ) represents the median of the mismatch distribution, μ the ‘per site per year’ mutation rate, and k the sequence length. We applied the mutation rate of 2.2-2.6%/Myr for crustacean mtDNA (Knowlton et al., 1993; Schubart et al., 1998). RESULTS A 672-bp segment of mitochondrial COI gene was amplified in 130 individuals from seven locations sampled. A total of 27 haplotypes were identified by 25 polymorphic sites, giving an overall nucleotide diversity of 0.00202 ± 0.00016, and haplotype diversity of 0.818 ± 0.032. Twenty haplotypes were identified from 60 Yellow Sea individuals; 19 haplotypes from 70 East China Sea individuals. All haplotype sequences were deposited in GenBank, accession numbers MF631999–MF632025. The most common haplotype (Hap6), shared by 53 individuals, might be ancestral in that it occurred at all Yellow and East China sea locations. Nucleotide diversity varied among populations, ranging 0.00167 ± 0.00036 (Y1) to 0.00278 ± 0.00064 (E4); haplotype diversity values were higher, ranging 0.772 ± 0.096 (Y1) to 0.848 ± 0.063 (Y2) (Table 1). Yellow Sea nucleotide and haplotype diversities were 0.00187 ± 0.00021 and 0.818 ± 0.049, respectively, whereas diversities ranged 0.00215 ± 0.00023 and 0.822 ± 0.042, respectively, across East China Sea locations. No clear geographic trend in COI gene diversity values was apparent. Genetic differentiation among populations was evaluated using FST values and AMOVA analyses. In general, pairwise FST values ranged −0.0362 (P = 0.9550) to 0.0008 (P = 0.1513) (Table 2), indicating a lack of genetic differentiation among populations. A low FST value between Yellow (Y1–Y3) and East China (E1–E4) seas populations also indicated a lack of obvious population genetic structure in the two seas. Table 2. Pairwise FST (below diagonal) and P (above diagonal) values among seven populations of Parapenaeopsis hardwickii from the Yellow Sea and East China Sea. Yellow Sea East China Sea Y1 Y2 Y3 E1 E2 E3 E4 Yellow Sea Y1 * 0.3514 0.4775 0.9189 0.5676 0.8469 0.1513 Y2 –0.0133 * 0.2252 0.6937 0.5496 0.6847 0.2865 Y3 –0.0116 –0.0033 * 0.6126 0.9369 0.5225 0.6847 East China Sea E1 –0.0264 –0.0146 –0.0110 * 0.9009 0.9550 0.5946 E2 –0.0031 –0.0163 –0.0280 –0.0248 * 0.8649 0.8108 E3 –0.0094 –0.0010 –0.0074 –0.0362 –0.0281 * 0.4955 E4 0.0008 0.0002 –0.0175 –0.0102 –0.0271 –0.0141 * Yellow Sea East China Sea Y1 Y2 Y3 E1 E2 E3 E4 Yellow Sea Y1 * 0.3514 0.4775 0.9189 0.5676 0.8469 0.1513 Y2 –0.0133 * 0.2252 0.6937 0.5496 0.6847 0.2865 Y3 –0.0116 –0.0033 * 0.6126 0.9369 0.5225 0.6847 East China Sea E1 –0.0264 –0.0146 –0.0110 * 0.9009 0.9550 0.5946 E2 –0.0031 –0.0163 –0.0280 –0.0248 * 0.8649 0.8108 E3 –0.0094 –0.0010 –0.0074 –0.0362 –0.0281 * 0.4955 E4 0.0008 0.0002 –0.0175 –0.0102 –0.0271 –0.0141 * View Large One-group AMOVA analysis revealed overall population differentiation to be −1.43% (P = 0.9198), and genetic variation within populations to be 101.43% (Table 3). AMOVA for the two groups (Yellow Sea and East China seas) revealed the source of genetic variation occurred within populations (101.52%, P = 0.9218), with variance between two groups and among populations within groups −0.21% (P = 0.7204) and −1.31% (P = 0.8954), respectively (Table 3). These results suggest no significant differences exist between Yellow Sea and East China Sea populations. Table 3. Analysis of molecular variance (AMOVA) for the mitochondrial COI gene haplotypes of Parapenaeopsis hardwickii in the Yellow Sea and East China Sea. Source of variation Variance components Percentage of variance F/φ-statistics p One gene pool Among populations –0.0058 –1.43 –0.0143 0.9198 Within populations 0.4138 101.43 Two gene pools (Yellow Sea and East China Sea) Between groups –0.0009 –0.21 –0.0021 0.7204 Among populations within groups –0.0053 –1.31 –0.0131 0.8954 Within populations 0.4138 101.52 –0.0152 0.9218 Source of variation Variance components Percentage of variance F/φ-statistics p One gene pool Among populations –0.0058 –1.43 –0.0143 0.9198 Within populations 0.4138 101.43 Two gene pools (Yellow Sea and East China Sea) Between groups –0.0009 –0.21 –0.0021 0.7204 Among populations within groups –0.0053 –1.31 –0.0131 0.8954 Within populations 0.4138 101.52 –0.0152 0.9218 View Large The Bayesian inference showed no phylogenetic structure in P. hardwickii, with low clade posterior probability (Fig. 2). Moreover, the median-joining network was characterized by a star-like phylogeny with closely related haplotypes derived from the most common and ancestral haplotype, rather than haplotypes dividing into geographical groups (Fig. 3). Figure 2. View largeDownload slide Bayesian inference tree constructed for COI gene haplotypes of Parapenaeopsis hardwickii. Parapenaeopsis tenella served as an outgroup (Pt). Figure 2. View largeDownload slide Bayesian inference tree constructed for COI gene haplotypes of Parapenaeopsis hardwickii. Parapenaeopsis tenella served as an outgroup (Pt). Figure 3. View largeDownload slide Median-joining network of haplotypes of Parapenaeopsis hardwickii. Sizes of circles are proportional to haplotype frequency. Perpendicular tick marks on the lines joining haplotypes represent the number of nucleotide substitutions; Yellow Sea (gray), East China Sea (black). Figure 3. View largeDownload slide Median-joining network of haplotypes of Parapenaeopsis hardwickii. Sizes of circles are proportional to haplotype frequency. Perpendicular tick marks on the lines joining haplotypes represent the number of nucleotide substitutions; Yellow Sea (gray), East China Sea (black). The mismatch distribution of P. hardwickii for the two seas presented a distinct unimodal curve, closely fitting expected distributions under a rapid population expansion model (Fig. 4). In addition, both Tajima’s D and Fu’s Fs test showed significant negative values (Table 4). These results suggest that P. hardwickii recently colonized, and then expanded in the Yellow Sea and East China Sea. Observed values of the age range expansion parameter (τ) were 1.426U and 1.531U of mutational time for the Yellow Sea and East China Sea, respectively. Based on the molecular clock for the COI gene the estimated time of population expansion into the Yellow Sea and East China Sea was 48,200-40,800 and 51,700-43,800 years ago, respectively. Figure 4. View largeDownload slide The observed pairwise differences (bars), and the expected mismatch distributions under the sudden expansion model (line) for the COI gene haplotypes in Parapenaeopsis hardwickii. Figure 4. View largeDownload slide The observed pairwise differences (bars), and the expected mismatch distributions under the sudden expansion model (line) for the COI gene haplotypes in Parapenaeopsis hardwickii. Table 4. Tajima’s D and Fu’s Fs, corresponding P value of Parapenaeopsis hardwickii. Sample Tajima’s D Fu’s Fs D P Fs P Yellow Sea (Y1-Y3) –2.0620 0.0020 –19.8494 < 0.0010 East China Sea (E1-E4) –1.9793 0.0050 –14.8993 < 0.0010 Pooled –2.0374 0.0020 –26.4864 < 0.0010 Sample Tajima’s D Fu’s Fs D P Fs P Yellow Sea (Y1-Y3) –2.0620 0.0020 –19.8494 < 0.0010 East China Sea (E1-E4) –1.9793 0.0050 –14.8993 < 0.0010 Pooled –2.0374 0.0020 –26.4864 < 0.0010 View Large DISCUSSION Marine organisms typically show low levels of genetic differentiation among geographical regions, owing to high dispersal potential and absence of physical barriers (Palumbi, 1994; Hewitt, 2000). Not surprisingly then, we found no difference in P. hardwickii genetic structure between the Yellow Sea and East China Sea populations. This life history of these species includes an offshore planktonic larval stage, estuarine post-larval and juvenile stages, and offshore benthic adult stage (Dall et al., 1990). Accordingly, high gene flow driven by ocean circulation might play an important role in maintaining population connectivity. Current circulation in the two seas is complex, including, the China Coastal Current, Yangtze River outflow, and Kuroshio tributary (Li et al., 2000). The China Coastal Current is known to transport floating marine organisms from the Yellow to the East and South China seas, such as fragments of the brown alga Sargassum and the copepod Calanus sinicus (Hwang & Wong, 2005; Cheang et al., 2010). Our results suggest larval P. hardwickii in the Yellow Sea and East China Sea might be similarly transported, contributing to gene flow between regions. Although freshwater runoff from the Yangtze River limits dispersal of the larvae of the limpet Cellana toreuma and the cocktail shrimp Trachypenaeus curvirostris along the Chinese coast (Dong et al., 2012; Han et al., 2015a), we found no evidence of this river restricting dispersal of the euryhaline P. hardwickii, a species tolerant to a wide salinity range (Shi et al., 2013). Several studies focusing on population genetic structure of Yellow and East China sea species (yellowfin drum, Nibea albiflora; gazami crab, Portunus trituberculatus; Chinese Venus clam, Cyclina sinensis; and two-spot swimming crab, Charybdis bimaculata) have found no significant genetic structure between the Yellow Sea and East China seas populations, indicating that egg, larval, and juvenile stages of each were tolerant of a wide range of Yangtze River outflow salinities (Feng et al., 2008; Han et al., 2008; Ni et al., 2012; Han et al., 2015b). These results reveal that the effect of the Yangtze River outflow on genetic structure is variable and depends, at least in part, on the habitat specificity and biological characteristics (e.g., salinity tolerance, dispersal ability) of species (Ni et al., 2014). Previous studies have suggested that P. hardwickii populations in the East China Sea and waters adjacent to Taiwan should be regarded as distinct (Tzeng et al., 2007; 2008). Surface current circulation in the Yellow Sea and East China Sea is counterclockwise, whereas it is clockwise in the South China Sea because of monsoonal drift. These opposing currents drive larval P. hardwickii in opposite directions, deepening divergence (Tzeng et al., 2007, 2008). Mismatch distribution analyses and neutrality tests (Fig. 4, Table 4) support the hypothesis of population expansion of P. hardwickii into the Yellow Sea and East China Sea. Based on mtDNA nucleotide and haplotype diversity values, Grant & Bowen (1998) proposed four basic population history scenarios. Prawns with low nucleotide and high haplotype diversities probably underwent sudden population expansion after a period of low effective population size. Following environmental disturbance, population size increased rapidly, with haplotype diversity recovering (usually via mutation), though nucleotide diversity remained low (given insufficient time to accumulate large sequence differences between haplotypes) (Avise, 2000; Lui et al., 2010). For P. hardwickii from the Yellow Sea and East China Sea, the expansion time was estimated to be 48,200-40,800 and 51,700-43,800 years ago, respectively. Compared to Pleistocene glacial–interglacial cycles, these expansion times are relatively close to periods of dramatic sea level fluctuation ~20,000–50,000 years ago (Waelbroeck et al., 2002). Previous phylogeographic studies have suggested that the sudden expansion of populations of marine species into the northwestern Pacific was a common event (Ni et al., 2014). During Pleistocene glacial cycles, fluctuations in sea level and water temperature were believed to have impacted the connectivity of populations of marine species. As one of the most extensive continental shelves in the northwestern Pacific, the Yellow Sea and most of the East China Sea were exposed during the late Quaternary glacial period, with the latter reduced to an elongated enclosed sea a third of its present area (Wang, 1999; Kitamura et al., 2001). Sword prawns in these marginal seas survived in common glacial refugia, but when sea levels rose as glaciers retreated in postglacial periods, prawns recolonized the Yellow Sea and East China Sea. Our studies also reveal a shallow and star-like topology, suggesting an origin from a common ancestral population in an East China Sea refugium. Our results revealed no significant genetic differentiation between the Yellow Sea and East China Sea populations of P. hardwickii, indicating a high level of gene flow between the two seas. Further studies of P. hardwickii throughout the West Pacific using more molecular markers would contribute to enhance our knowledge of its genetic structure and evolutionary history, thus providing scientific basis and information for conserving wild germplasm resources. ACKNOWLEDGEMENTS This research was financially supported by the National Natural Science Foundation of China (grant 41506173). We are very much indebted to Dong Dong, Lin Ma, Jixing Sui, Qi Kou, Zhibin Gan, Lin Gong, Jinbao Wang, Yueyun Wang, Yong Xu, and Yue Sun, for their assistance in the field and laboratory. We also thank the anonymous reviewers for their comments to the manuscript, and Liwen Bianji, Edanz Group China for editing the English text of a draft of the manuscript. REFERENCES Alam, M.M.M., De Croos, M.D.S.T. & Pálsson, S. 2017. Mitochondrial DNA variation reveals distinct lineages in Penaeus semisulcatus (Decapoda, Penaeidae) from the Indo-West Pacific Ocean. Marine Ecology , 38: e12406. Google Scholar CrossRef Search ADS Alam, M.M.M., Westfall, K.M. & Pálsson, S. 2015. Mitochondrial DNA variation reveals cryptic species in Fenneropenaeus indicus. Bulletin of Marine Science , 91: 15– 31. Google Scholar CrossRef Search ADS Alam, M.M.M., Westfall, K.M. & Pálsson, S. 2016. Mitogenomic variation of Bangladesh Penaeus monodon (Decapoda: Panaeidae) and reassessment of its phylogeography in the Indo-West Pacific region. Hydrobiologia , 763: 249– 265. Google Scholar CrossRef Search ADS Avise, J.C. 2000. Phylogeography: The history and formation of species . Harvard University Press, Cambridge, MA, USA. Bandelt, H.J., Forster, P. & Rohl, A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution , 16: 37– 48. Google Scholar CrossRef Search ADS PubMed Cheang, C.C., Chu, K.H. & Ang, P.O. 2010. Phylogeography of the marine macroalga Sargassum hemiphyllum (Phaeophyceae, Heterokontophyta) in northwestern Pacific. Molecular Ecology , 19: 2933– 2948. Google Scholar CrossRef Search ADS PubMed Dall, W., Hill, B.J., Rothlisberg, P.C. & Sharples, D.J. 1990. The biology of the Penaeidae . Academic Press, London. De Bruyn, M., Nugroho, E., Hossain, M.M., Wilson, J.C. & Mather, P.B. 2005. Phylogeographic evidence for the existence of an ancient biogeographic barrier: the Isthmus of Kra Seaway. Heredity , 94: 370– 378. Google Scholar CrossRef Search ADS PubMed Dong, Y.W., Wang, H.S., Han, G.D., Ke, C.H., Zhan, X., Nakano, T. & Williams, G.A. 2012. The impact of Yangtze river discharge, ocean currents and historical events on the biogeographic pattern of Cellana toreuma along the China coast. PLoS ONE , 7: e36178. Google Scholar CrossRef Search ADS PubMed Excoffier, L. & Lischer, H.E. 2010. Arlequin suite version 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources , 10: 564– 567. Google Scholar CrossRef Search ADS PubMed Excoffier, L., Smouse, P.E. & Quattro, J. M. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics , 131: 479– 491. Google Scholar PubMed Feng, B.B., Li, J.L., Niu, D.H., Chen, L., Zheng, Y.F. & Zheng, K.H. 2008. Compared analysis on the sequences of Mitochondrial CR Gene and COI Gene Fragments of nine wild stocks of Portunus trituberculatus from the marginal seas of China. Chinese Journal of Zoology , 43: 28– 36. Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology , 3: 294– 299. Google Scholar PubMed Fu, Y.X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics , 147: 915– 925. Google Scholar PubMed Grant, W.S. & Bowen, B.W. 1998. Shallow population histories in deep evolutionary lineages of marine fishes: Insights from sardines and anchovies and lessons for conservation. Journal of Heredity , 89: 415– 426. Google Scholar CrossRef Search ADS Han, Z.Q., Gao, T.X., Takashi, Y. & Yasunori, S. 2008. Genetic population structure of Nibea albiflora in Yellow Sea and East China Sea. Fisheries Science , 74: 544– 552. Google Scholar CrossRef Search ADS Han, Z.Q., Zhu, W.B., Zheng, W., Li, P. & Shui, B.N. 2015a. Significant genetic differentiation between the Yellow Sea and East China Sea populations of cocktail shrimp Trachypenaeus curvirostris revealed by the mitochondrial DNA COI gene. Biochemical Systematics and Ecology , 59: 78– 84. Google Scholar CrossRef Search ADS Han, Z.Q., Zheng, W., Chen, G.B., Shui, B.N., Liu, S.F. & Zhuang, Z.M. 2015b. Population genetic structure and larval dispersal strategy of portunid crab Charybdis bimaculata in Yellow sea and East China sea. Mitochondrial DNA , 26: 402– 408. Google Scholar CrossRef Search ADS Hewitt, G.M. 2000. The genetic legacy of the Quaternary ice ages. Nature , 405: 907– 913. Google Scholar CrossRef Search ADS PubMed Hwang, J.S. & Wong, C.K. 2005. The China Coastal Current as a driving force for transporting Calanus sinicus (Copepoda: Calanoida) from its population centers to waters off Taiwan and Hong Kong during the winter northeast monsoon period. Journal of Plankton Research , 27: 205– 210. Google Scholar CrossRef Search ADS Kitamura, A., Takano, O., Takata, H. & Omote, H. 2001. Late Pliocene-early Pleistocene paleoceanographic evolution of the Sea of Japan. Palaeogeography, Palaeoclimatology, Palaeoecology , 172: 81– 98. Google Scholar CrossRef Search ADS Kong, L.F. & Li, Q. 2009. Genetic evidence for the existence of cryptic species in an endangered clam Coelomactra antiquata. Marine Biology , 156: 1507– 1515. Google Scholar CrossRef Search ADS Knowlton, N., Weight, L.A., Solórzano, L.A., Mills, D.K. & Bermingham, E. 1993. Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science , 260: 1629– 1632. Google Scholar CrossRef Search ADS PubMed Li, N.S., Zhao, S.L. & Wasiliev, B. 2000. Geology of marginal sea in the Northwest Pacific . Heilongjiang Education Press, Harbin, China [in Chinese]. Librado, P. & Rozas, J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics , 25: 1451– 1452. Google Scholar CrossRef Search ADS PubMed Liu, J.X., Gao, T.X., Wu, S.F. & Zhang, Y.P. 2007. Pleistocene isolation in the Northwestern Pacific marginal seas and limited dispersal in a marine fish, Chelon haematocheilus (Temminck and Schlegel, 1845). Molecular Ecology , 16: 275– 288. Google Scholar CrossRef Search ADS PubMed Liu, Y.S., Shi, Y.H., Zhang, G.Y., Xu, J.B., Xie, Y.D., Yan, Y.L. & Lu, G.H. 2013. Effects of salinity on serum ions and digestive enzyme activities of Parapenaeopsis hardwickii. Journal of Shanghai Ocean University , 22: 206– 211 [in Chinese]. Lui, K.K.Y., Leung, P.T.Y., Ng, W.C. & Leung, K.M.Y. 2010. Genetic variation of Oratosquilla oratoria (Crustacea: Stomatopoda) across Hong Kong waters elucidated by mitochondrial DNA control region sequences. Journal of the Marine Biological Association of the United Kingdom , 90: 623– 631. Google Scholar CrossRef Search ADS Miers, E.J., 1878. Notes on the Penæidæ in the collection of the British Museum, with descriptions of some new species. Proceedings of the Zoological Society of London , 1878: 298– 310, pl. 17. Ni, G., Li, Q., Kong, L.F. & Zheng, X. 2012. Phylogeography of bivalve Cyclina sinensis: Testing the historical glaciations and Changjiang River outflow hypotheses in northwestern Pacific. PLoS ONE , 7: e49487. Google Scholar CrossRef Search ADS PubMed Ni, G., Li, Q., Kong, L.F. & Yu, H. 2014. Comparative phylogeography in marginal seas of the northwestern Pacific. Molecular Ecology , 23: 534– 548. Google Scholar CrossRef Search ADS PubMed Palumbi, S.R. 1994. Genetic divergence, reproductive isolation, and marine speciation. Ecology, Evolution, and Systematics , 25: 547– 572. Posada, D. 2008. jModelTest: phylogenetic model averaging. Molecular Biology & Evolution , 25: 1253– 1256. Google Scholar CrossRef Search ADS Rogers, A.R. & Harpending, H. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology & Evolution , 9: 552– 569. Ronquist, F. & Huelsenbeck, J.P. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics , 19: 1572– 1574. Google Scholar CrossRef Search ADS PubMed Schubart, C.D., Diesel, R. & Hedges, S.B. 1998. Rapid evolution to terrestrial life in Jamaican crabs. Nature , 393: 363– 365. Google Scholar CrossRef Search ADS Shen, K.N., Jamandre, B. W., Hsu, C.C., Tzeng, W.N. & Durand, J.D. 2011. Plio-Pleistocene sea level and temperature fluctuations in the northwestern Pacific promoted speciation in the globally-distributed flathead mullet Mugil cephalus. BMC Evolutionary Biology , 11: 1– 17. Google Scholar CrossRef Search ADS PubMed Shi, Y.H., Zhang, G.Y., Liu, Y.S., Yan, Y.L., Xie, Y.D., Lu, G.H., Xu, J.B. & Liu, J.Z. 2013. Effects of salinity on nutrient composition，amino acid composition and content in the muscle of Parapenaeopsis hardwickii. Chinese Journal of Zoology , 48: 399– 406 [in Chinese]. Song, H.T. & Ding, T.M. 1993. A comparative study on fishery biology of main economic shrimps in the north of East China Sea. Journal of Zhejiang Ocean University , 12: 240– 248 [in Chinese]. Song, H.T., Yu, C.G. & Xue, L.J. 2009. Study on the biomass distribution and growth property of Parapenaeopsis hardwickii in the East China Sea. Acta Hydrobiologica Sinica , 33: 15– 21 [in Chinese]. Google Scholar CrossRef Search ADS Su, J.L. & Yuan, Y.L. 2005. Coastal hydrology of China . Ocean Press, Beijing. [in Chinese] Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics , 123: 585– 595. Google Scholar PubMed Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research , 24: 4876– 4882. Google Scholar CrossRef Search ADS Tzeng, T.D. 2007. Population structure of the Sword Prawn (Parapenaeopsis hardwickii) (Decapoda: Penaeidae) in the East China Sea and waters adjacent to Taiwan inferred from the Mitochondrial Control Region. Zoological Studies , 46: 561– 568. Tzeng, T.D., Chu, T.J., Wang, D., Haung, H.L. & Yeh, S.Y. 2008. Population structure in the Sword Prawn (Parapenaeopsis hardwickii) from the East China Sea and Taiwan Strait inferred from intron sequences. Journal of Crustacean Biology , 28: 234– 239. Google Scholar CrossRef Search ADS Waelbroeck, C., Labeyrie, L., Michel, E., Duplessy, J.C., McManus, J.F., Lambeck, K., Balbon, E. & Labeyrie, M. 2002. Sea-level and deep water temperature changes derived from benthic foraminifera isotopic records. Quaternary Science Reviews , 21: 295– 305. Google Scholar CrossRef Search ADS Wang, P.X. 1999. Response of western Pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features. Marine Geology , 156: 5– 39. Google Scholar CrossRef Search ADS Wei, C.D. 1991. Fauna Zhejiang: crustaceans . Zhejiang Science and Technology Press, Hangzhou, China [in Chinese]. Zhang, C.J., Yao, G.X., Wu, G.J., Ren, Z.H. & Chen, A.H. 2011. The technique study of artificial breeding for Parapenaeopsis hardwickii. Fisheries Science & Technology Information , 38: 281– 283 [in Chinese]. © The Author(s) 2017. Published by Oxford University Press on behalf of The Crustacean Society. All rights reserved. For permissions, please e-mail: firstname.lastname@example.org
The Journal of Crustacean Biology – Oxford University Press
Published: Jan 1, 2018
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