Next Article in Journal
Transcriptome Analysis Reveals Cross-Tissue Metabolic Pathway Changes in Female Rana dybowskii during Emergence from Hibernation
Previous Article in Journal
Effects of Myo-Inositol on the Growth Performance, Digestive Enzyme Activity, and Antioxidation of Juvenile Hucho taimen
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Fishes
Volume 8
Issue 12
10.3390/fishes8120568
fishes-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Microsatellite-Marker-Based Evaluation of Stock Enhancement for Kuruma Prawn Penaeus japonicus in Beibu Gulf, South China Sea

by
Mengyi Zhang
1,2,
Yu Zhao
1,3,
Binbin Shan
1,3,
Yan Liu
1,3,
Changping Yang
1,3,
Liangming Wang
1,3,
Manting Liu
1,3,
Qijian Xie
1,3,
Yuan Li
4,
Jianwei Zou
5,* and
Dianrong Sun
1,3,*
1
South China Sea Fisheries Research Institute, Chinese Academy of Fisheries Sciences, Guangzhou 510300, China
2
School of Fishery, Zhejiang Ocean University, Zhoushan 316022, China
3
Key Laboratory of Marine Ranching, Ministry of Agriculture Rural Affairs, Guangzhou 510300, China
4
Third Institute of Oceanography, Ministry of Natural Resources, Xiamen 361005, China
5
Beihai Fishery Technology Extension Station, Beihai 536000, China
*
Authors to whom correspondence should be addressed.
Fishes 2023, 8(12), 568; https://doi.org/10.3390/fishes8120568
Submission received: 18 October 2023 / Revised: 18 November 2023 / Accepted: 20 November 2023 / Published: 22 November 2023
Browse Figures
Versions Notes

Abstract

:
The objectives of this study were to evaluate the effect of stock enhancement on Penaeus japonicus (Bate, 1888) in Beibu Gulf, South China Sea, and to investigate whether stock enhancement has genetically affected the natural population of P. japonicus in the Beibu Gulf waters. Five microsatellite loci were used to identify released individuals among recaptured specimens. In total, 13 of the 487 recaptured individuals were found with their corresponding parents for this release of shrimp seedlings, accounting for 2.67% of the total recaptured P. japonicus. Furthermore, it was determined that the genetic differences among the broodstock, released, and recaptured populations of P. japonicus were small and did not cause significant changes in the genetic structure of P. japonicus in the area. In conclusion, the stock enhancement of P. japonicus in Beibu Gulf had a certain effect on resource restoration, and there is no difference in the genetic characteristics obtained by the microsatellite markers compared to the original population in this area.
Keywords:
Penaeus japonicus; stock enhancement; population genetic differentiation; parentage assignments; genetic diversity
Key Contribution: Our research demonstrated that the total contribution rate of the stock enhancement of Penaeus japonicus in Beibu Gulf was 2.67%. In addition, the stock enhancement population of P. japonicus did not produce significant changes in the genetic structure of the population in the area.

Graphical Abstract

1. Introduction

Stock enhancement is an effective way to facilitate the recovery of fishery resources, which means that artificially cultivated seedlings or temporarily cultivated natural seedlings of varying sizes are artificially released into natural waters for the purpose of restoring or increasing the number of aquatic organisms in order to achieve the rapid replenishment of fishery resources [1,2]. Thus far, although stock enhancement has achieved good results in some countries, the external tagging technique used to assess the effects of stock enhancement has some limitations, and the external tags easily fall off, which greatly affects assessments of the released population proportion in wild populations [3]. In addition, the genetic characteristics of the released seedlings themselves largely affect the genetic diversity of wild populations in target waters [4], so the genetic monitoring of both released and wild populations provides a basis for the future survival and development of the populations as well as contributes to the maintenance of local species diversity.
The Kuruma prawn, Penaeus japonicus (Bate, 1888), is widely distributed in the Indo-West Pacific, mainly in the East and South China Seas; around the southern part of Hokkaido, Japan; near Southeast Asia; north of Australia; near the eastern part of Africa; and in the Red Sea [5]. This species is tolerant to low temperatures, has a fast growth rate, has high nutritional and economic value, is well liked, and is an important aquaculture species worldwide [6].
The production of P. japonicus in China was approximately 54,792 tons in 2010 [7]. However, due to the lack of parental shrimp numbers caused by overfishing and the lack of attention to shrimp selection and genetic improvement as well as habitat degradation and other factors, shrimp resources in natural waters have declined drastically, with the annual production of P. japonicus in China dropping to 45,949 tons by 2013 [8]. Therefore, to restore the natural resources of P. japonicus, stock enhancement was gradually expanded in the following years. Together with the government’s increased investment related to stock enhancement, the management policies related to the stock enhancement of P. japonicus were gradually standardized and updated, and the benefits of stock enhancement returns for this species were improved [9]. By 2017, the release of P. japonicus in the Shandong Peninsula region had exceeded 20 × 108 tails, with a yield of up to 3500 tons [9].
However, despite the scale of the stock enhancement increase, there are still few studies on genetic monitoring and genetic diversity before and after enhancement. Wei et al. (2016) assessed the stock enhancement of P. japonicus in the waters near Xiangshan Port using mitochondrial markers. Comparing the genetic diversity levels of the three populations, the broodstock, released, and recaptured populations, it was concluded that the populations of released and recaptured P. japonicus maintained a high level of genetic diversity, with no significant differences in variation and no differentiation between the populations, suggesting that stock enhancement is one of the more effective measures to maintain the amount of P. japonicus stock resources at present [10]. When genetic exchange occurs between the released population and the wild population, it may cause changes in the genetic structure of the population within the natural environment; therefore, it is particularly important to study the genetic diversity of the P. japonicus population before and after stock enhancement [11,12].
Microsatellites (microsatellite DNA), also known as simple sequence repeats (SSRs), simple tandem repeats (STRs), or simple sequences, are composed of repeated DNA motifs (usually 1–6 base pairs) [13,14]. They have many advantages as molecular markers: high polymorphism, genetic codominance, easy detection, and low requirements for template DNA compared with that for other genetic markers [15]. They can be used for population genetics [16,17,18,19], pedigree analysis [20,21,22], and population genetic-map construction [23,24,25]. Microsatellite markers are also important in aquaculture, contributing to the conservation and improvement of aquaculture species through the genetic analysis of the species, helping to understand species diversity, phylogeny, evolution, and development and providing a basis for the sustainable conservation and development of aquaculture [26,27,28].
In this study, we used microsatellite molecular markers to identify released individuals among recaptured specimens and calculated the recapture rate of P. japonicus to preliminarily assess the release of P. japonicus in the Beibu Bay, China. The genetic differences between the broodstock, released, and recaptured populations of P. japonicus were also determined to analyse the genetic effects of stock enhancement.

2. Materials and Methods

2.1. Sample Collection

In April 2019, 134 P. japonicus females (with mature gonads) were collected for artificial breeding in the waters near Beihai, South China Sea, and approximately 5 million P. japonicus offspring were successfully bred. In May 2019, the offspring were released in the stock enhancement area. In Figure 1, the star indicates the location of the release site. In addition, before release, a certain number of broodstock and released populations was collected for morphological measurements, and shrimp tail muscle tissue was excised and preserved in 95% ethanol for back up. After release, monthly recaptures of P. japonicus were conducted from August to November 2019 at five sampling sites: A (21°35′24″ N, 108°7′48″ E), B (21°43′48″ N, 108°33′36″ E), C (21°27′36″ N, 109°19′48″ E), D (21°18′36″ N, 109°17′24″ E), and E (21°16′48″ N, 109°37′48″ E). The sampling sites are shown in Figure 1, and detailed sampling information is given in Table 1. Morphological measurements were taken on the P. japonicus recapture population, and tail muscle tissue was excised and preserved in 95% ethanol for DNA extraction and subsequent genetic analysis.

2.2. DNA Extraction and PCR Amplification

A total of 134 P. japonicus broodstock individuals, 48 released individuals, and 487 selected recaptured individuals was used for the evaluation of the stock enhancement effect and the genetic study of the natural population. Five microsatellite loci with high polymorphism were selected [29]. Three fluorescent markers were used, carboxytetramethylrhodamine (TAM), carboxyfluorescein (FAM), and hexachloro fluorescein (HEX). Tagged primers were designed by linking three fluorescent markers to the 5’ end of the forward primer on five microsatellite loci. Specific DNA extraction and PCR amplification steps were performed as described by Zhao et al. (2020) [30].

2.3. Data Analysis

Released individual identification was performed by using the software Cervus 3.0 [31]. The parameters of each microsatellite locus, namely, number of alleles (Na), observed heterozygosity (Ho), expected heterozygosity (He), polymorphism information content (PIC), and frequency of null alleles F(Null), and the proportion of excluded nonreleased individuals, i.e., the theoretical exclusion rate (PE) measured by the software in the simulated case, were counted. The theoretical exclusion rate is mainly used to assess the genetic identification ability of a pair of primers. The probability of not excluding an incorrect parent is NE-1P when the genotype of the candidate’s single parent is known. The software POPGENE 3.2 [32] was used to calculate Na, Ho, He, and PIC of microsatellite loci in each population. The allelic richness (RS) was obtained using FSTAT 2.9.3 [33] software, and the genetic differentiation index FST between two populations was calculated and tested for significance via 1000 random samplings. Population 1.2 [34] was used to calculate the genetic distances between the three P. japonicus populations according to the criteria of Nei et al. (1983) [35].

3. Results

3.1. Microsatellite-Marker Polymorphism and Parentage Assignments

The polymorphism results of the microsatellite markers at the five loci showed 143 alleles (Na), with an average allele number of 28.6 alleles per locus. The maximum number of alleles was found for the CSPJ002 locus, 40 alleles, and the minimum number of alleles was found for the CSPJ015 locus, 13 alleles. The polymorphism information content (PIC) was 0.654–0.968, the observed heterozygosity (Ho) was 0.382–0.867, the average observed heterozygosity was 0.694, the expected heterozygosity (He) was 0.673–0.970, and the average expected heterozygosity was 0.874 (Table 2). The simulation analysis performed by Cervus showed that the nonexclusion probability (first parent) of NE-1P was 0.112–0.703, and the combined nonexclusion probability was 0.0019. Thus, the theoretical exclusion rate (PE-1P) of the five microsatellites was 99.81% (Table 2).

3.2. Identification of Released Individuals among Recaptured Individuals

The theoretical basis for parentage identification is Mendel’s law of inheritance, which states that the two alleles of the offspring at a microsatellite locus are from two parents. A simulation analysis was done using the software Cervus to estimate the parentage identification ability of each locus based on the allele situations of each locus obtained. The identification of the released individuals and the exclusion of the nonreleased individuals in the P. japonicus recapture individuals were performed. The results showed that 474 nonreleased individuals were excluded from the 487 recaptured individuals, which accounted for 97.33% of the total number of recaptured individuals. Another 13 individuals were matched to the corresponding female parent at the five microsatellite loci and were identified as released individuals, accounting for 2.67% of the total number of recaptured individuals; the highest percentage of recaptures occurred in August 2019, when 7 of the 171 recaptured individuals were released individuals, representing 4.09% of the total number of recaptured individuals. The percentage of recapture was lower in September and November 2019 at zero. There were some differences in the percentage of recapture at different recapture times (Table 3).

3.3. Genetic Diversity

The total numbers of alleles at the five microsatellite loci for the three P. japonicus populations were 95, 64, and 141 (Table 4). The average number of alleles ranged from 12 (released population) to 28.2 (recaptured population); the average allele abundance (RS) was 12.641 (released population) to 19.325 (recaptured population); and the polymorphism information content (PIC) ranged from 0.819 (recaptured population) to 0.824 (broodstock population), except for the CSPJ015 locus, which had a slightly lower PIC in the recaptured population. The PIC values of all the loci were approximately the same, and they all indicated a high level of genetic diversity. The average expected heterozygosity (0.841 and 0.850) of the broodstock population and the released population of P. japonicus showed that both populations had high genetic diversity and that seedling breeding for stock enhancement did not result in reduced genetic diversity. The analysis of the inbreeding coefficient Fis showed that this coefficient was negative at the CSPJ010 locus in the released population and positive in the rest of the P. japonicus populations, indicating the severe inbreeding or mixing of differentiated populations between these populations.

3.4. Population Genetic Differentiation

The results of the FST analysis of the genetic differentiation indices among the three populations of P. japonicus using the five microsatellite molecular markers showed significant and weak genetic differentiation between the broodstock population and the released population. In contrast, we observed higher genetic differentiation between the recaptured population and the others. The genetic distance analysis showed similar results: the genetic distance between the released population and the broodstock population was the smallest (0.189), while the genetic distance between the recaptured population and the other two populations was the largest (Table 5).

4. Discussion

The South China Sea straddles the tropics and subtropics, with rich and diverse habitats and high species diversity. Benefiting from these conditions, several fishing grounds have been formed in the South China Sea region, and the Beibu Gulf fishing ground is one of the famous fishing grounds in the South China Sea [36]. Due to the increasing fishing pressure in recent years, the amount of fishery resources in Beibu Gulf has declined significantly, with the amount of fishery resources in 2016–2017 being only one-fifth of that in 1961–1962, and the fishery resources are in serious decline [37]. To restore the resources of P. japonicus in the waters of the South China Sea and Beibu Gulf, artificially bred shrimp seedlings were released in this study for resource restoration, and the effect of stock enhancement was assessed by using microsatellite molecular markers.

4.1. Effect of the P. japonicus Stock Enhancement Programme

The assessment of stock enhancement effects is an important measure for the effective management of stock enhancement, and the assessment results can be used as a basis for improving the technical methods of stock enhancement and providing better technical support for the recovery of fishery resources [38]. The use of molecular-marker technology has become one of the most effective means for the accurate and long-term assessment of stock enhancement effects [39]. Parameters such as Na, He, Ho, and PIC provide important information on the genetic diversity and parentage assignment of populations [40]. Botstein et al. (1980) concluded that microsatellite markers with He > 0.6 and PIC > 0.5 are the most plausible discriminators [41]. In the present study, the five microsatellite loci yielded an average Ho of 0.694, an average He of 0.874, and an average PIC of 0.865, indicating that the polymorphism at the five microsatellite markers used in the present experiment was high; i.e., a higher accuracy could be obtained in the parentage analysis. In this study, the combined exclusion probability was 0.998 in the parentage assignment analysis, which further confirmed the accuracy of this experiment and the high confidence level of the experimental results. In addition, Luan et al. (2006) compared the genetic variations between wild and cultured P. japonicus collected from Xiamen using six pairs of microsatellite markers [42]. The PIC values ranged from 0.6701 to 0.8989, with average Ho values ranging from 0.6935 (cultured population) to 0.7370 (wild population) and average He values ranging from 0.8169 (wild population) to 0.8209 (cultured population); the genetic diversity was at a high level. The results of this study are consistent with those of Luan et al. and indicate that the P. japonicus populations in this study also had a high level of genetic diversity.
The issue of adequate genetic markers is of paramount importance in the methodology of marine fishery genetics [43,44,45,46,47,48]. It was clearly shown that neutral markers are not enough to make a conclusion about genetic changes in the population structure of marine organisms [48,49]. It could be correspondingly concluded that neutral genetic markers are not enough to assess the influence of stock enhancement on the genetic composition of the P. japonicus natural population. It might happen that there are some significant changes in the P. japonicus natural population which can be detected with adaptive markers but not with neutral markers like microsatellite loci. Therefore, more certainty about the impact of aquaculture on the P. japonicus natural populations will be possible after genetic studies using adaptive markers.
In this study, we evaluated the stock enhancement activity of P. japonicus in May 2019 and studied the P. japonicus recaptured from August to November 2019 based on microsatellite markers to assess the stock enhancement effect in 2019. Among 487 recaptured individuals, 13 individuals were identified as released individuals, resulting in a recapture rate of 2.67%. In Japan, the recapture rates of P. japonicus used for stock enhancement were reported to range from approximately 0.0% to 22.1% in 40 cases but exceeded 10% in only 2 cases [50]. This result shows that the recapture rate after stock enhancement in Japan was mostly below 10%, consistent with the results of this study. On the other hand, in China, Mei et al. (2010) evaluated the stock enhancement of P. japonicus in Laoshan Bay in 2008 using indicators such as the recapture rate [51]. The results showed that its recapture rate was 0.48%. Jiang et al. (2012) assessed the effectiveness of P. japonicus stock enhancement in Xiangshan Harbour and showed that the recapture rate was 0.25% [52]. Compared with the recapture rate in the Chinese study, the recapture rate obtained in this paper was slightly higher, and the possible reasons for this are as follows: five pairs of microsatellites were used for released individual identification; additionally, there may be a bias between the identification results and the actual recapture results, so the number of markers should be increased appropriately to allow for the better approximation of the actual rate. Furthermore, Beibu Gulf is a marginal inner bay in the Western Pacific Ocean which provides a good habitat for P. japonicus; additionally, P. japonicus do not migrate long distances, so there is a higher chance of catching released individuals in the stock enhancement area.

4.2. Genetic Effects of Stock Enhancement

Stock enhancement may have an impact on the genetic characteristics of the target marine species, and the artificial breeding stock released into the natural environment may alter the genetic diversity of the wild population; e.g., intraspecific competition occurs between the released population and the natural population, and if the released population dominates in bouts of intraspecific competition, the size of the natural population will decrease. A corresponding reduction in genetic diversity will occur [53]. The introduction of novel pathogens into the natural environment via the released breeding population may result in higher mortality in the wild population due to a lack of immunity to the novel pathogens, which will lead to a reduction in the size of the wild population and, consequently, a reduction in the level of genetic diversity in the natural population. The released population can also alter the genetic characteristics of the wild population via genetic exchange with this population [4]. Therefore, in this study, the genetic diversity among the broodstock population, the released population, and the recaptured population was analysed. The results for the three P. japonicus populations in our study at the five microsatellite loci showed that the average He ranged from 0.830 to 0.850, the average Ho ranged from 0.585 to 0.747, and the average PIC ranged from 0.819 to 0.824. To investigate the genetic structure of P. japonicus populations and to improve genetic breeding, Guo et al. (2011) studied three wild populations of P. japonicus using ten pairs of microsatellite primers [54]. The results showed that the average PIC of the three populations ranged from 0.6507 to 0.5569, the average He ranged from 0.6189 to 0.7193, and the average Ho ranged from 0.4661 to 0.6243, indicating that all three wild populations had a high level of genetic diversity. The overall values reported in this paper were slightly higher than those of Guo et al., indicating that the three P. japonicus populations in this study also had a high level of genetic diversity.
The inbreeding coefficient Fis can be used as a measure of intraspecific inbreeding [55]. In this study, Fis was negative for the released population at the CSPJ010 locus, but for the rest of the population, each locus showed positive values, indicating the serious inbreeding or mixing of differentiated populations among the three populations of P. japonicus. It is hypothesized that this is due to the limited number of parents used by the farms during the breeding of seedlings. When these individuals enter the natural environment, gene exchange occurs between them and the wild population, resulting in changes in the genetic structure of the population within the natural environment [56,57]. Therefore, in the future stock enhancement programmes of shrimps, attention should be given to strengthening the control of the seedling breeding process, using sufficient numbers of parents, and optimizing the mating pattern to reduce the impact of inbreeding depression on stock enhancement. The levels of genetic differentiation among populations are usually measured by the genetic distance and genetic differentiation coefficient [15]. According to the genetic differentiation index (Fst) analysis, there was significant genetic differentiation among the broodstock population, the released population, and the recaptured population. If the genetic differentiation between released and natural populations is significant, it may lead to changes in the genetic structure of the P. japonicus populations in natural waters, which should be avoided [57]. This may be because a sufficient number of parents from the target waters were not used to breed the shrimp seedlings, which diminished the similarity with the genetic background of the wild populations. More wild populations from the target waters should be introduced as broodstock to increase the diversity of released populations and to prevent greater genetic differentiation from natural populations.
The results of this study together showed that the released P. japonicus population did not have a significant demographic or genetic impact, evaluated with microsatellite markers, on the natural population. However, if the resources and ecological balance of P. japonicus are to be maintained in the long term, the continuous genetic monitoring of natural populations using more molecular markers is required; more attention should be given to the possible effects on the genetic aspects of the natural population to achieve the sustainable use of its resources.

5. Conclusions

In this study, we used microsatellite molecular markers to identify released individuals among recaptured specimens and calculated the recapture rate of P. japonicus to preliminarily assess the release of P. japonicus in Beibu Bay, China. The genetic differences between the broodstock, the released population, and the recaptured population of P. japonicus were also determined to analyse the genetic effects of stock enhancement. Among the 487 recaptured individuals, 13 individuals were identified as released individuals, resulting in a recapture rate of 2.67%. The results of this study together showed that the released P. japonicus population did not have a significant genetic impact, evaluated with microsatellite markers, on the natural population. However, if the resources and ecological balance of P. japonicus are to be maintained in the long term, the continuous genetic monitoring of natural populations using more molecular markers is required.

Author Contributions

Conceptualization, M.Z. and Y.Z.; data curation, B.S. and Y.L. (Yan Liu); formal analysis, Y.Z., C.Y. and L.W.; funding acquisition, J.Z. and D.S.; investigation, M.Z., Y.Z. and Q.X.; methodology, M.Z., B.S., Y.L. (Yan Liu) and J.Z.; project administration, J.Z. and D.S.; resources, Y.L. (Yan Liu) and C.Y.; software, M.Z. and B.S.; supervision, L.W., J.Z. and D.S.; validation, M.L.; visualization, D.S.; writing—original draft preparation, Y.Z. and M.Z.; writing—review and editing, M.Z. and Y.L. (Yuan Li). All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the National Natural Science Foundation of China (42206109); the Central Public-interest Scientific Institution Basal Research Fund, South China Sea Fisheries Research Institute, CAFS (NO. 2023RC03); the Central Public-interest Scientific Institution Basal Research Fund CAFS (NO. 2023TD93); and China–Vietnam Fishery Stock Enhancement and Conservation in Beibu Gulf.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The data presented in this study are available in this article.

Acknowledgments

We are grateful to Xiaoling Chen for her help in our sequencing work.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analysis, or interpretation of the data; in the writing of the manuscript; or in the decision to publish the results.

Correction Statement

This article has been republished with a minor correction to the title. This change does not affect the scientific content of the article.

References

  1. Bell, J.D.; Bartley, D.M.; Lorenzen, K.; Loneragan, N.R. Restocking and stock enhancement of coastal fisheries: Potential, problems and progress. Fish. Res. 2006, 80, 1–8. [Google Scholar] [CrossRef]
  2. Lorenzen, K.; Leber, M.K.; Blankenship, L.H. Responsible approach to marine stock enhancement: An update. Rev. Fish. Sci. 2010, 18, 189–210. [Google Scholar] [CrossRef]
  3. Shan, B.B.; Liu, Y.; Song, N.; Yang, C.P.; Liu, S.N.; Gao, T.X.; Sun, D.R. Parentage determination of black sea bream (Acanthopagrus schlegelii) for stock enhancement: Effectiveness and loss of genetic variation. Acta Oceanol. Sinica. 2021, 40, 41–49. [Google Scholar] [CrossRef]
  4. Escalante, M.A.; García-De-León, F.J.; Dillman, C.B.; de los Santos Camarillo, A.; George, A.; Barriga-Sosa, I.D.L.A.; Manel, S. Genetic introgression of cultured rainbow trout in the Mexican native trout complex. Conserv. Genet. 2014, 15, 1063–1071. [Google Scholar] [CrossRef]
  5. Ren, X.; Yu, Z.; Xu, Y.; Zhang, Y.; Mu, C.; Liu, P.; Li, J. Integrated transcriptomic and metabolomic responses in the hepatopancreas of kuruma shrimp (Marsupenaeus japonicus) under cold stress. Ecotoxicol. Environ. Saf. 2020, 206, 111360. [Google Scholar] [CrossRef] [PubMed]
  6. Xu, J.; Li, F.; Zhang, J.; Wang, L.; Liu, X.; Xue, W.; Shi, Y.; Cui, Y. The interleukin enhancer binding factor-2 (ILF2) gene in Penaeus japonicus shrimp: Cloning, tissue distribution, and antiviral effects. Aquacult. Int. 2023; in press. [Google Scholar]
  7. Bureau MOAA. 2021 China Fishery Statistical Yearbook; China Agriculture Press: Beijing, China, 2021. [Google Scholar]
  8. Bureau MOAA. 2014 China Fishery Statistical Yearbook; China Agriculture Press: Beijing, China, 2014. [Google Scholar]
  9. Lu, L. Enhancement and release of marine fishery resources and their fishery benefits. Agric. Technol. Equipm 2020, 371, 132–133. (In Chinese) [Google Scholar]
  10. Wei, H.Q.; Zhang, F.G.; Jiang, K.J.; Jiang, Y.Z.; Meng, Y.Y.; Song, W.; Ma, C.Y.; Cheng, J.H.; Ma, L.B. Genetic diversity analysis of Marsupenaeus japonicus population for reproduction and release. J. Fish. Sci. 2016, 23, 530–537. [Google Scholar]
  11. Sekino, M.; Hara, M.; Taniguchi, N. Loss of microsatellite and mitochondrial DNA variation in hatchery strains of Japanese flounder Paralichthys olivaceus. Aquaculture 2002, 213, 101–122. [Google Scholar] [CrossRef]
  12. Liu, W.L.; Liu, B.W.; Liu, Q.; Wang, H. The overview of genetic and ecology impacts on stock enhancemnet. Anhui. Agric. Sci. Bull. 2020, 26, 68–70. (In Chinese) [Google Scholar]
  13. Homchan, S.; Bhadola, P.; Gupta, Y.M. Statistical Analysis of Simple Sequence Repeats in Genome Sequence: A Case of Acheta Domesticus (Orthoptera: Gryllidae). ECS Trans. 2022, 107, 14799. [Google Scholar] [CrossRef]
  14. Zhong, S.; Chen, W.; Yang, H.; Shen, J.; Ren, T.; Li, Z.; Tan, F.Q.; Luo, P. Characterization of microsatellites in the Akebia trifoliata genome and their transferability and development of a whole set of effective, polymorphic, and physically mapped simple sequence repeat markers. Front. Plant Sci. 2022, 13, 860101. [Google Scholar] [CrossRef]
  15. Du, J.; Hou, C.; Chen, X.; Xiao, J.; Gul, Y.; Wang, H. Morphometric analysis and fluorescent microsatellite markers to evaluate the genetic diversity of five populations of Penaeus japonicus in China. Aquacult. Fish. 2022, 7, 321–327. [Google Scholar] [CrossRef]
  16. White, S.L.; Kazyak, D.C.; Darden, T.L.; Farrae, D.J.; Lubinski, B.A.; Johnson, R.L.; Eackles, M.S.; Balazik, M.T.; Brundage, H.M., III; Fox, A.G.; et al. Establishment of a microsatellite genetic baseline for North American Atlantic sturgeon (Acipenser o. oxyrhinchus) and range-wide analysis of population genetics. Conserv. Genet. 2021, 22, 977–992. [Google Scholar] [CrossRef]
  17. Wang, H.; Yang, B.; Wang, H.; Xiao, H. Impact of different numbers of microsatellite markers on population genetic results using SLAF-seq data for Rhododendron species. Sci. Rep. 2021, 11, 8597. [Google Scholar] [CrossRef] [PubMed]
  18. Alavi-Siney, S.M.; Saba, J.; Nasiri, J. Genetic variability and population genetic structure in autotriploid saffron using allelic phenotypes of microsatellite markers. Sci. Hortic. 2022, 299, 111043. [Google Scholar] [CrossRef]
  19. Song, N.; Li, P.; Zhang, X.; Gao, T. Changing phylogeographic pattern of Fenneropenaeus chinensis in the Yellow Sea and Bohai Sea inferred from microsatellite DNA: Implications for genetic management. Fish. Res. 2018, 200, 11–16. [Google Scholar] [CrossRef]
  20. Weng, Z.; Yang, Y.; Wang, X.; Wu, L.; Hua, S.; Zhang, H.; Meng, Z. Parentage analysis in giant grouper (Epinephelus lanceolatus) using microsatellite and SNP markers from genotyping-by-sequencing data. Genes 2021, 12, 1042. [Google Scholar] [CrossRef]
  21. Wang, Q.; Hu, Q.; Yang, S.; Li, Y. Isolation of tetrameric microsatellite markers and its application on parentage identification in Procambarus clarkii. Aquacult. Int. 2023, 31, 2099–2111. [Google Scholar] [CrossRef]
  22. Forsdick, N.J.; Cubrinovska, I.; Massaro, M.; Hale, M.L. Microsatellite genotyping detects extra-pair paternity in the Chatham Island Black Robin, a highly inbred, socially monogamous passerine. Emu-Austral Ornithol. 2021, 121, 68–74. [Google Scholar] [CrossRef]
  23. Ma, H.; Yu, D.; Li, J.; Qin, Y.; Zhang, Y.; Yu, Z. Construction of first genetic linkage map based on microsatellite markers and characterization of di-and tri-nucleotide microsatellite markers for Crassostrea hongkongesis. Aquaculture 2022, 556, 738272. [Google Scholar] [CrossRef]
  24. Romanov, M.N.; Da, Y.; Chemnick, L.G.; Thomas, S.M.; Dandekar, S.S.; Papp, J.C.; Ryder, O.A. Towards a genetic linkage map of the California condor, an endangered New World vulture species. Animals 2022, 12, 3266. [Google Scholar] [CrossRef] [PubMed]
  25. Wenne, R. Microsatellites as molecular markers with applications in exploitation and conservation of aquatic animal populations. Genes 2023, 14, 808. [Google Scholar] [CrossRef] [PubMed]
  26. Herkenhoff, M.E.; Bajay, M.M.; Costamilan, C.A.D.V.L. Genetic structure and biodiversity in wild Centropomus parallelus and in wild and recently domesticated Centropomus undecimallis populations. Life 2023, 13, 1595. [Google Scholar] [CrossRef]
  27. Tesfaye, G.; Curto, M.; Meulenbroek, P.; Englmaier, G.K.; Tibihika, P.D.; Alemayehu, E.; Getahun, A.; Meimberg, H. Genetic diversity of Nile tilapia (Oreochromis niloticus) populations in Ethiopia: Insights from nuclear DNA microsatellites and implications for conservation. BMC. Ecol. Evol. 2021, 21, 113. [Google Scholar] [CrossRef]
  28. Zhao, Y.; Zhu, X.; Li, Z.; Xu, W.; Dong, J.; Wei, H.; Li, Y.; Li, X. Genetic diversity and structure of Chinese grass shrimp, Palaemonetes sinensis, inferred from transcriptome-derived microsatellite markers. BMC Genet. 2019, 20, 75. [Google Scholar] [CrossRef]
  29. Moore, S.S.; Whan, V.; Davis, G.P.; Byrne, K.; Hetzel, D.J.; Preston, N. The development and application of genetic markers for the Kuruma prawn Penaeus japonicus. Aquaculture 1999, 173, 19–32. [Google Scholar] [CrossRef]
  30. Zhao, Y.; Sun, D.R.; Shan, B.B.; Liu, Y.; Yang, C.P.; Zhou, W.L. Comparison and analysis of genetic variation between the released population and the population in the breeding area of Pagrus major based on microsatellite markers. Mar. Sci. 2020, 44, 66–73. (In Chinese) [Google Scholar]
  31. Marshall, T.C.; Slate, J.; Kruuk, L.; Pemberton, J.M. Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 1998, 7, 639–655. [Google Scholar] [CrossRef]
  32. Yeh, F.C.; Yang, R.C.; Boyle, T.B.J.; Ye, Z.H.; Mao, J.X. POPGENE, the user-friendly shareware for population genetic analysis. Mol. Biol. Biotechnol. Cent. 1997, 10, 295–301. [Google Scholar]
  33. Goudet, J. FSTAT, Version 2.9.3: A Program to Estimate and Test Gene Diversities and Fixation Indices. 2001. Available online: http://www.unil.ch/izea/softwares/fstat.html (accessed on 7 January 2021).
  34. Olivier, L. Populations 1.2. 2002. Available online: http://www.cnrs-gif.fr/pge/bioinfo/populations/ (accessed on 7 January 2021).
  35. Nei, M.; Tajima, F.; Tateno, Y. Accuracy of estimated phylogenetic trees from molecular data: II. Gene frequency data. J. Mol. Evol. 1983, 19, 153–170. [Google Scholar] [CrossRef]
  36. Chen, Z.Z.; Lin, Z.J.; Qiu, Y.S. Evaluation of sustainability of fisheries resources for South China Sea based on the AHP. J. Nat. Resour. 2010, 25, 249–257. [Google Scholar]
  37. Su, L.; Chen, Z.Z.; Zhang, K.; Xu, Y.W.; Qiu, Y.S. Establishment of quality status evaluation system of fishery resources in Beibu Gulf based on bottom trawl survey data. J. Guangdong Ocean Univ. 2021, 41, 10–16. [Google Scholar]
  38. Liu, L.; Lin, L.; Li, C.H.; Liu, Y.; Xu, S.N.; Zhou, Y.B. Effect assessment of marine fishery stock enhancement: A review of the literature. Guangdong Agr. Sci. 2014, 41, 133–137 + 143. [Google Scholar]
  39. Guo, A.; Yuan, J.L.; Lian, Q.P.; Ni, M.; Liu, M.; Gu, Z.M. Stock enhancement effect and potential genetic risks of Xenocypris davidi by molecular markers in the upper reaches of Qiantang River, China. J. Fish. China 2022, 46, 2349–2356. [Google Scholar]
  40. Seo, D.; Bhuiyan, M.S.A.; Sultana, H.; Heo, J.M.; Lee, J.H. Genetic diversity analysis of South and East Asian duck populations using highly polymorphic microsatellite markers. Asian Austral. J. Anim. 2016, 29, 471–478. [Google Scholar] [CrossRef]
  41. Botstein, D.; White, R.L.; Skolnick, M.; Davis, R.W. Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am. J. Hum. Genet. 1980, 32, 314–331. [Google Scholar]
  42. Luan, S.; Kong, J.; Wang, Q.Y. Genetic variation of wild and cultured populations of the Kuruma prawn Marsupenaeus japonicus (Bate 1888) using microsatellites. Aquacult. Res. 2006, 37, 785–792. [Google Scholar] [CrossRef]
  43. Nielsen, E.E.; Hemmer-Hansen, J.A.K.O.B.; Larsen, P.F.; Bekkevold, D. Population genomics of marine fishes: Identifying adaptive variation in space and time. Mol. Ecol. 2009, 18, 3128–3150. [Google Scholar] [CrossRef]
  44. Corander, J.; Majander, K.K.; Cheng, L.; Merilä, J. High degree of cryptic population differentiation in the Baltic Sea herring Clupea harengus. Mol. Ecol. 2013, 22, 2931–2940. [Google Scholar] [CrossRef]
  45. Gagnaire, P.A.; Broquet, T.; Aurelle, D.; Viard, F.; Souissi, A.; Bonhomme, F.; Arnaud-Haond, S.; Bierne, N. Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era. Evol. Appl. 2015, 8, 769–786. [Google Scholar] [CrossRef]
  46. Bekkevold, D.; Gross, R.; Arula, T.; Helyar, S.J.; Ojaveer, H. Outlier loci detect intraspecific biodiversity amongst spring and autumn spawning herring across local scales. PLoS ONE 2016, 11, e0148499. [Google Scholar] [CrossRef] [PubMed]
  47. Liu, B.J.; Zhang, B.D.; Xue, D.X.; Gao, T.X.; Liu, J.X. Population structure and adaptive divergence in a high gene flow marine fish: The small yellow croaker (Larimichthys polyactis). PLoS ONE 2016, 11, e0154020. [Google Scholar] [CrossRef] [PubMed]
  48. Allendorf, F.W.; Luikart, G.; Aitken, S.N. Conservation and the Genetics of Populations, 2nd ed.; Wiley-Blackwell Publishing: Oxford, UK, 2013; Volume 602, p. 46. [Google Scholar]
  49. Hauser, L.; Carvalho, G.R. Paradigm shifts in marine fisheries genetics: Ugly hypotheses slain by beautiful facts. Fish. Fish. 2008, 9, 333–362. [Google Scholar] [CrossRef]
  50. Hamasaki, K.; Kitada, S. A review of kuruma prawn Penaeus japonicus stock enhancement in Japan. Fish. Res. 2006, 80, 80–90. [Google Scholar] [CrossRef]
  51. Mei, C.; Ren, Y.P.; Xu, B.D.; Fan, Y.C. Preliminary study on the effect of Penaeus japonicus bate releasing in the Laoshan Bay. Period. Ocean Univ. China 2010, 40, 45–50. [Google Scholar]
  52. Jiang, Y.; Ling, J.; Lin, N.; Yuan, X.; Li, S. Stocking effectiveness of hatchery-released kuruma prawn Penaeus japonicus in the Xiangshan Bay, China. Shengtai Xuebao/Acta Ecol. Sin. 2012, 32, 2651–2658. (In Chinese) [Google Scholar]
  53. Romo, O.V.; Suzuki, S.; Nakajima, M.; Taniguchi, N. Genetic evaluation of interindividual relatedness for brood stock management of the rare species barfin flounder Verasper moseri using microsatellite DNA markers. Fish. Sci. 2006, 72, 33–39. [Google Scholar] [CrossRef]
  54. Guo, H.; Shen, Y.C. Genetic diversity analysis of three wild populations of Marsupenaeus japonicus using SSR technique. Fish. Sci. 2011, 21, 42–43. [Google Scholar]
  55. Tong, X.; Gong, S.Y.; Yu, D.H.; Huang, G.J.; Du, B.; Li, S.D. Genetic diversity of cultured pacific white shrimp (Litopenaeus vannamei) stocks of different generations in China. Oceanol. Limnol. Sin. 2009, 40, 214–220. [Google Scholar]
  56. Liu, B.; Zhang, X.; Wang, Z.; Li, W.; Zhang, Q.; Liu, Q.; Li, W.; Zhang, L.; Liu, Y.; Wang, C. Genetic pattern fluctuations in wild swimming crab populations, under the influence of continuous mass stock enhancement. Fish. Res. 2021, 243, 106075. [Google Scholar] [CrossRef]
  57. Liu, Q.; Li, C.; Li, W.; Gao, R.; Liu, B.; Liu, W.; Yi, G.; Zhang, L.; Li, M.; Su, J. Genetic identification of Chinese shrimp Fenneropenaeus chinensis post-release in Jinzhou Bay: Implications for management of stock enhancement. Reg. Stud. Mar. Sci. 2022, 53, 102425. [Google Scholar] [CrossRef]
Fishes 08 00568 g001
Figure 1. Map showing the locations of sampling sites. Sampling sites of P. japonicus. The recaptured population was sampled at sites indicated by black circles, and the star indicates the location of the release site.
Figure 1. Map showing the locations of sampling sites. Sampling sites of P. japonicus. The recaptured population was sampled at sites indicated by black circles, and the star indicates the location of the release site.
Fishes 08 00568 g001
Table 1. Sample information of P. japonicas.
Table 1. Sample information of P. japonicas.
Recapture Time
(month/year)		Recapture SiteNumber of Total SamplesNumber of Genotyped Individuals
August 2019C230171
September 2019B8682
October 2019A, B, D, E239221
November 2019D1813
Total–573487
Table 2. Genetic diversity and parentage assignment parameters of five microsatellite loci.
Table 2. Genetic diversity and parentage assignment parameters of five microsatellite loci.
LocusNaHoHePICF(Null)NE–1P
CSPJ002400.7640.9530.9500.1120.173
CSPJ015130.3820.6730.6540.2950.112
CSPJ010190.8670.8950.8850.0150.703
CSPJ012220.6930.8780.8660.1180.295
CSPJ008490.7640.9700.9680.1200.353
Mean28.60.694 0.874 0.865 ––
Note: Na, number of alleles; Ho, observed heterozygosity; He, expected heterozygosity; PIC, polymorphism information content; F(Null), frequency of null alleles; and NE-1P, nonexclusion probability (first parent).
Table 3. The rate of released P. japonicus in recapture samples.
Table 3. The rate of released P. japonicus in recapture samples.
Recapture Date (month/year)Recapture SizeReleased IndividualsRate
August 201917174.09%
September 20198200
October 201922152.26%
November 20191300
Total487132.67%
Table 4. Main polymorphic parameters for five microsatellite loci applied in this study.
Table 4. Main polymorphic parameters for five microsatellite loci applied in this study.
nParametersLocusAverage
CSPJ002CSPJ015CSPJ010CSPJ012CSPJ008
Broodstock
population		134Na27914182719
Ho0.4850.7310.8120.6240.2730.585
He0.8750.7660.8430.8990.8230.841
RS21.2027.892 12.39114.40522.81315.741
Fis0.4470.0460.0370.3070.6700.306
PIC0.8650.7320.8240.8860.8130.824
Released
population		48Na2059121812
Ho0.9150.6670.9380.6040.6100.747
He0.9330.7750.8210.8280.8900.850
RS19.6945.0008.82911.68318.00012.641
Fis0.0200.141–0.1440.2720.3180.122
PIC0.9190.7290.7870.7990.8690.821
Recaptured
population		487Na401319204928.2
Ho0.8440.2820.8830.7120.8790.720
He0.9580.5010.8870.8290.9740.830
RS27.8977.30812.62612.69636.09719.325
Fis0.1190.4360.0040.1420.0980.132
PIC0.9550.4810.8750.8090.9730.819
Note: n, sample size; Na, number of alleles; RS, allele richness; He, expected heterozygosity; Ho, observed heterozygosity; PIC, polymorphism information content; and Fis, inbreeding coefficient.
Table 5. Pairwise FST (below diagonal) and genetic distance (above diagonal) values among P. japonicus populations (* p < 0.05).
Table 5. Pairwise FST (below diagonal) and genetic distance (above diagonal) values among P. japonicus populations (* p < 0.05).
Broodstock PopulationRecaptured PopulationReleased Population
Broodstock population–0.3310.189
Recaptured population 0.126 *–0.498
Released population0.031 *0.133*–
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Zhang, M.; Zhao, Y.; Shan, B.; Liu, Y.; Yang, C.; Wang, L.; Liu, M.; Xie, Q.; Li, Y.; Zou, J.; et al. Microsatellite-Marker-Based Evaluation of Stock Enhancement for Kuruma Prawn Penaeus japonicus in Beibu Gulf, South China Sea. Fishes 2023, 8, 568. https://doi.org/10.3390/fishes8120568

AMA Style

Zhang M, Zhao Y, Shan B, Liu Y, Yang C, Wang L, Liu M, Xie Q, Li Y, Zou J, et al. Microsatellite-Marker-Based Evaluation of Stock Enhancement for Kuruma Prawn Penaeus japonicus in Beibu Gulf, South China Sea. Fishes. 2023; 8(12):568. https://doi.org/10.3390/fishes8120568

Chicago/Turabian Style

Zhang, Mengyi, Yu Zhao, Binbin Shan, Yan Liu, Changping Yang, Liangming Wang, Manting Liu, Qijian Xie, Yuan Li, Jianwei Zou, and et al. 2023. "Microsatellite-Marker-Based Evaluation of Stock Enhancement for Kuruma Prawn Penaeus japonicus in Beibu Gulf, South China Sea" Fishes 8, no. 12: 568. https://doi.org/10.3390/fishes8120568

APA Style

Zhang, M., Zhao, Y., Shan, B., Liu, Y., Yang, C., Wang, L., Liu, M., Xie, Q., Li, Y., Zou, J., & Sun, D. (2023). Microsatellite-Marker-Based Evaluation of Stock Enhancement for Kuruma Prawn Penaeus japonicus in Beibu Gulf, South China Sea. Fishes, 8(12), 568. https://doi.org/10.3390/fishes8120568

Article Metrics

Back to TopTop