Population genetic structure of the sword prawn Parapenaeopsis hardwickii (Miers, 1878) (Decapoda: Penaeidae) in the Yellow Sea and East China Sea

Population genetic structure of the sword prawn Parapenaeopsis hardwickii (Miers, 1878)... 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 5.0.0.1 (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. 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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: journals.permissions@oup.com http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png The Journal of Crustacean Biology Oxford University Press

Population genetic structure of the sword prawn Parapenaeopsis hardwickii (Miers, 1878) (Decapoda: Penaeidae) in the Yellow Sea and East China Sea

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Abstract

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 5.0.0.1 (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. 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Published: Jan 1, 2018

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