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Article

Population Genetic Structure with Mitochondrial DNA of the Chub Mackerel Scomber japonicus in Korean Coastal Waters

Department of Marine Biology and Aquaculture, The Institute of Marine Industry, Gyeongsang National University, Tongyeong 53064, Republic of Korea
J. Mar. Sci. Eng. 2025, 13(2), 252; https://doi.org/10.3390/jmse13020252
Submission received: 26 December 2024 / Revised: 22 January 2025 / Accepted: 26 January 2025 / Published: 29 January 2025
(This article belongs to the Special Issue Ocean Observations)

Abstract

:
Scomber japonicus, commonly known as chub mackerel, is a fish species of economic significance in Korea, China, and Japan, whose natural abundance has reduced dramatically due to overfishing and environmental changes. To investigate the genetic differentiation and population structure of S. japonicus, a 359 base pair segment of the mitochondrial DNA (mtDNA) control region sequence was analyzed in 96 individuals sampled from three locations in Korean waters. Sixty-six haplotypes were recognized, of which 61 (92.42%) were population specific, whereas only five haplotypes were shared by multiple populations (8%). Two clades were revealed with low support values, and no specific genealogical branches were recognized according to geographical locations. Significant genetic differentiations, however, were detected among the three populations, with FST values (p < 0.05). These results indicate that populations of S. japonicus in Korean waters are genetically subdivided. Migration patterns, spawning site fidelity, and current temperature could be the possible causes of this subdivision. Consequently, it is thought that each of the genetically unique S. japonicus stocks found in Korean waters requires a different approach to management.

1. Introduction

Chub mackerel Scomber japonicus (Perciformes: Scombridae) is a widely distributed coastal pelagic fish found from the surface to a depth of 300 m, inhabiting the tropical and temperate waters of the Atlantic, Indian, and Pacific oceans and adjacent seas, and is particularly abundant in Korea, China, Japan, and California in the USA [1,2]. Scomber japonicus inhabiting the Tsushima Warm Current is commercially important in Korea, China, and Japan and is caught mainly by purse seine fisheries [3]. Although S. japonicus is distributed throughout the Korean waters, more than 80% of the fish is caught in the South Sea of Korea. Since the 1990s, the abundance of S. japonicus has been low [3]. In Korea, the catch of S. japonicus reached its peak at 400 × 103 mt in 1990 and then reduced to about 15 × 103 mt in recent years [4] due to overfishing or climatological change. A consistent descending trend was observed in the CPUE (Catch Per Unit Effort) data for S. japonicus along the Korean waters between 1994 and 2021 [5]. Furthermore, it was also reported that a one-degree increase in sea surface temperature (SST) would lead to a 13% decrease in total catch of pelagic fish [6]. However, the SST in Korean waters has increased by 1.44 °C over the past 56 years since 1968 [7].
To ensure sustainable use and management of fishery resources, Korea has instituted a TAC (Total Allowable Catch) and designated one month during the S. japonicus spawning season as a closed season [8]. The spawning season of S. japonicus ranges from April to June [9,10]. Among the several spawning grounds of the Tsushima Warm Current Stock, two major spawning grounds are located in the South Sea of South Korea [3]. However, S. japonicus spawns along the whole Korean coast [11,12]. The species usually migrates between spawning and feeding grounds. They usually move northward to the East Sea and western part of Korea during the warm season for feeding and return towards the South Sea for overwintering and spawning [3,13]. However, little is known about the gene flow between the populations in the West (Yellow Sea), South, and East Seas of Korea, and there is not enough molecular data to conclude whether they are a single biological unit or not.
Cheng et al. [14] conducted an experiment with mitochondrial DNA (mtDNA) control region, but only one sample from Korea (Jeju Island) was used in that study and found no structured population. Yan et al. [15] conducted an experiment with mtDNA control region and found genetic differentiation between the Japanese and Chinese populations. On the other hand, an experiment with microsatellites, including samples from China and Japan, revealed a structured population, but no samples from Korea were included in this study [16]. Therefore, in Korea, sufficient research with molecular markers to ascertain the genetic differentiation and population genetic structure is yet to be undertaken.
The use of mtDNA markers has proven to be useful for assessing the barriers to gene flow in widespread marine species that were previously believed to be homogeneous. Among the different types of markers, the mtDNA control region shows a remarkably fast pace of nucleotide substitution and a high level of intraspecific polymorphism [17,18], which has been proven to be sensitive to detect genetic diversity and population genetic structure [19]. In this study, the mtDNA control region was used with the objective to determine the genetic differentiation and population genetic structure of S. japonicus, inhabiting the West, South, and East Seas of Korea.

2. Materials and Methods

2.1. Sample Collection

A total of 96 individuals were collected from three locations of Korean waters in 2013. To accurately assess the haplotype and nucleotide variation, 32 individuals were sampled from each location [20]. Morphological characters were used to identify every individual collected from different locations. Mature fish were carefully selected for this study during the spawning season to ensure genetic stock integrity. The names of the locations are Geomundo (SJG) from the South Sea, Kangrung (SJK) from the East Sea, and Boryeong (SJB) from the West Sea (Figure 1, Table 1). After collection, samples were stored at −80 °C in the laboratory. Muscle samples from each individual were dissected and preserved in 95% ethanol for DNA extraction.

2.2. DNA Extraction, Amplification, and Sequencing

Total DNA was extracted from 96 S. japonicus muscle tissues preserved in 95% ethanol using the Wizard genomic DNA purification kit (Promega, Madison, WI, USA). To amplify the mtDNA CR region, universal primers H-16498 (5′-CCTGAAGTAGGAACCAGATC-3′) [21] and L-15924 (5′-AGCTCAGCGCCAGAGCGCCGGTCTTCTAAA-3′) [22] were used. PCR was carried out in 15 μL reactions containing 0.6 μL of template DNA, 1.5 μL of 10XTaq DNA polymerase buffer (Takara, Otsu, Japan), 1.5 μL of each 5 μmol primer, 1.5 μL of 2.5 mM dNTP, and 0.1 μL of Ex Taq DNA polymerase (Takara). PCR was performed with an initial denaturation for 6 min at 94 °C, annealing for 1 min at 54 °C, a 2 min extension at 72 °C, and a final extension for 7 min at 72 °C. A mixture of 3 µL of PCR product and 4 µL of 6XLoading buffer was injected into a 1.5% agarose gel and operated for 30 min at 100 volts in an electrophoresis device. After completion of the reaction, the product was stained with ethidium bromide for 40 min to confirm that the total DNA was extracted. The PCR product was purified by mixing 0.5 µL of ExoSAP-IT (United States Biochemical Corporation, Cleveland, OH, USA) and 1.5 µL of sterile water and reacting for 15 min at 80 °C and then 30 min at 37 °C. The nucleotide sequence was obtained using an ABI BigDye terminator cycle sequencing kit version 3.1 (Applied Biosystems Inc., Waltham, MA, USA) on an ABI PRISM 3130 genetic analyzer (Applied Biosystems Inc., Waltham, MA, USA).

2.3. Data Analysis

Sequences were aligned and edited by Bioedit V7.0.8 software [23]. A neighbor-joining (NJ) tree was created with the MEGA 5.05 [24] software by 1000 bootstrap replication, using outgroup S. australasicus. A haplotype network was constructed to observe the intraspecific relationship among haplotypes with Arlequin 3.5.1.2 and HapStar v.0.7 software program [25]. Arlequin version 3.5.1.2 [26] was used to calculate genetic parameters, including the number of polymorphic sites, nucleotide diversity, number of haplotypes, and haplotype diversity. Genetic differences among populations were detected by fixation index (FST) with 1000 replications. To investigate the deviation from neutrality, Tajima’s D test [27] and Fu’s Fs test [28] were selected, which could assess the expansion of population. Demographic history of population expansion was further investigated by mismatch distribution, which is based on three parameters: θ0 and θ1 (which represent before and after the population growth, respectively) and τ (time since expansion expressed in units of mutational time [29]). Harpending’s raggedness index (Hri) and sum of squared deviations (SSD) were calculated to observe the validity of expected and observed mismatch distribution. The values of τ generated by mismatch distribution analysis were transformed to estimate the expansion time with the equation τ = 2ut [29], in which u is the mutation rate per sequence per generation and t is the time since expansion. A divergence rate of 5–10% Ma−1 was used to estimate the time since expansion [30,31].

3. Results

A 359 bp segment of the mtDNA control region was obtained from 96 individuals, collected from three locations (Boryeong, Geomundo, and Kangrung) in Korean waters. Sequence analysis of the 359 bp mtDNA control region revealed 66 haplotypes with 29 polymorphic sites, including transitions and transversions of 20 and 9, respectively, and no indels were observed. All haplotypes were registered in GenBank with accession numbers MW561492–MW561557. A majority of the haplotypes (92.42%) were population-specific and were found in only one population. The numbers of population-specific haplotypes found in Boryeong, Geomundo, and Kangrung were 13, 23, and 24, respectively. Two haplotypes (SJB032 and SJB021) were shared by all populations, and three haplotypes (SJB017, SJB028, and SJB024) were shared by two populations. Within the population, haplotype diversity ranged from 0.948 (0.023) in Boryeong to 0.990 (0.010) in Kangrung. The nucleotide diversity ranged from 0.012 (0.007) in Boryeong to 0.016 (0.008) in Geomundo and Kangrung. Genetic diversity indices, including polymorphic sites, number of haplotypes, haplotype diversity, and nucleotide diversity, are presented in Table 1.
A neighbor-joining tree was constructed based on the haplotypes of S. japonicus mtDNA control region. The neighbor-joining tree of this species revealed that 66 haplotypes were assigned to two different clades, but bootstrap supports were low. The haplotypes of clade 1 and clade 2 were 40 (61 individuals) and 26 (35 individuals), respectively, with 22 polymorphic sites in each clade. The haplotype diversity was 0.972 (0.011) and 0.980 (0.013), whereas nucleotide diversity was 0.011 (0.006) and 0.008 (0.004), respectively, for clade 1 and clade 2 (Table 1). The distributions of the haplotypes from both clades are presented in Table 2. Neither clade exhibited any genealogical branches according to geographical locations (Figure 2). Further investigations of the geographical relationship were observed by a minimum spanning network (Figure 3). The minimum spanning tree had a starlike topology, where many rare haplotypes were radiating from some common haplotypes, suggesting population expansion. The results of the neutrality test and the mismatch distribution are presented in Table 3. Fu’s Fs test, which is considered sensitive for population expansion determination, was negative and significant for all populations, as well as for clade 1 and clade 2, indicating population expansion. The mismatch distribution for clade 1 and clade 2 was unimodal (Figure 4), which is supported by the low and insignificant Harpending raggedness index and the sum of squared deviation. The expansion times for clades 1 and 2 were estimated to be 61,000–244,000 and 38,000–158,000 years ago, respectively, before the present.
Genetic differentiation of the S. japonicus populations was carried out by estimating pairwise FST values. The pairwise FST comparison of the three populations was significant (0.053–0.075, p < 0.05), indicating the restriction of gene flow among the populations (Table 4).

4. Discussion

The mtDNA control region is thought to be an especially sensitive marker for marine species when it comes to understanding genetic diversity and population genetic structure. The level of haplotype and nucleotide diversity observed in this study is typical of marine fishes in the northwestern Pacific Ocean [32,33,34]. The haplotype and nucleotide diversity observed in the present study were relatively higher than those in the previous study, conducted by Yan et al. [15] and Cheng et al. [16], suggesting that S. japonicus maintains a larger effective population size in Korean waters [18] despite overfishing. The Boryeong population exhibited comparatively lower haplotype diversity, nucleotide diversity, and population specific haplotypes than the other two populations in Korea. Boryeong is not an ideal spawning ground for S. japonicus, which may affect its recruitment. The wild population in this area could be drastically reduced because of overfishing compared to its biomass, which may reduce its genetic diversity [35,36].
High haplotype and nucleotide diversity indicates that the species is either stable or that it has originated from a previously differentiated population [37]. Although bootstrap values were low, two distinct clades were identified. Fs test, which is sensitive to demographic expansion [28], was negative and significant for the two clades, indicating population expansion. On the other hand, unimodal mismatch distribution along with low and insignificant SSD and Hri also suggested that both the clades had undergone demographic expansion [29]. The minimum spanning tree also suggested congruent population expansion for S. japonicus. The sharing of the haplotypes of both clades in all populations suggested that these populations originated from an admixture of two differentiated populations. Within a species, the presence of two different mitochondrial clades is assumed to be the consequence of secondary contact and interbreeding of populations after being isolated geographically for a relatively long time [38]. The presence of two clades was also observed in a previous study conducted by Cheng et al. [16]. In several other marine fishes, such as Thamnaconus modestus [39], Scomberomorus niphonius [32], and Coilia nasus, co-occurrence of differentiated mtDNA lineages has been revealed [40].
S. japonicus is considered a species sensitive to environmental changes [41]. The estimation of the expansion time for the two clades was consistent with the previous study indicating a late Pleistocene period expansion. Drastic changes during the Pleistocene glacial period can influence the abundance and distribution of marine fishes by leading to migration to a suitable area or by causing mortality without leaving their genes [42]. Due to the drop in the sea level of about 120–140 m during the Pleistocene period, including the Last Glacial Maximum, vast areas of the Yellow Sea, East China Sea, and the coastal area of Korea were exposed, and the East Sea was almost detached from its surroundings [43,44]. As a result, living habitats as well as breeding grounds could have been lost, which forced them to survive in the refugia. The present populations around the Korean coast could have been established by the expansion of the surviving populations from different refugia after the glaciers receded due to the rise in temperature [45].
Marine fishes typically show low levels of genetic partitions among different geographic regions because of the absence of physical barriers, dispersal, or migration of larvae, juveniles, and adults at different life stages [37,46]. Our observed results were in contrast to the characteristics of S. japonicus. Pairwise comparisons among all the populations were significant for S. japonicus. A majority of the haplotypes (92.42%) were found to be population-specific, which also indicated the restriction of gene flow [47]. Moreover, the population-specific haplotype with high frequency and absence or over-representation in shared haplotypes also supports the genetic distinctiveness of these populations. These results contradict the previous findings of Cheng et al. [14]. On the other hand, Cheng et al. [16] and Yan et al. [15] found genetically differentiated groups with microsatellite and mtDNA control region markers, respectively. However, many other marine pelagic fish species also have a genetically differentiated population despite having high larval dispersal and large effective population size [48,49]. The biological behavior of marine fishes, migration patterns, spawning grounds specificity, and interaction with the oceanographic environment are important factors that may influence the genetic differentiation among populations of a species such as S. japonicus [16,49]. The species exhibits different migration patterns to some degree in different regions. Fish from the northern part of the South China Sea are characterized by short-distance migration. On the other hand, S. japonicus of the Yellow Sea and the Bohai Sea show a differentiated structure from the southern East China Sea with different migration routes, spawning grounds, and spawning times [16,50]. Kim et al. [12] found a difference in spawning time between the southwestern East Sea and southern West Sea with Jeju Island in the South Sea of Korea. Therefore, genetic variation between the three populations may occur due to the spawning site fidelity. Genetic differentiation among the populations in the Korean coastal waters has also been observed for other migratory fish, such as Gadus macrocephalus, because of spawning site fidelity, observed in the mtDNA control region and microsatellite [51]. Bekkevold et al. [49] also found a differentiated population for highly migratory fish with pelagic larvae, Clupea harengus, due to spawning site fidelity, and site fidelity was assumed to be caused by environmental differences. The southern coast of Korea is directly influenced by the Tsushima Warm Current with high temperatures in summer [52], which may form a front with the west and east coasts of Korea. Kim et al. [12] assumed that spawning of S. japonicus occurs at different times at different locations in Korea due to the sensitivity of the eggs and larvae to temperature. Li et al. [53] reported that S. japonicus larvae that enter unfavorable areas experience reduced growth and can potentially die. Therefore, temperature could be a barrier for dispersion, as also suggested for S. japonicus [16] and Lateolabrax maculatus [36]. It is also suggested that the dispersion of larvae by the ocean current also leads to a high death rate [54], as they have to overcome environmental differences.
S. japonicus in Korean waters exhibits high genetic diversity compared to the findings of a previous study. In addition, genetic differentiation among the population was observed, which is unusual for pelagic migratory species such as S. japonicus. However, complex oceanic patterns, spawning site fidelity, and differences in migration patterns support these findings. According to our findings, the current management units that are thought to be a single stock are actually made up of several genetically different stocks. To ensure their sustainability, these populations might need separate management policies and require a re-evaluation of Korea’s current fishery monitoring system.

Funding

This research was supported by Korea Institute of Marine Science & Technology Promotion (KIMST) grant funded by the Ministry of Oceans and Fisheries (KIMST RS-2021-KS211500, Korea-Arctic Ocean Warming and Response of Ecosystem, KOPRI, and RS-2023-00256330, Development of risk managing technology tackling ocean and fisheries crisis around Korean Peninsula by Kuroshio Current).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author due to privacy.

Conflicts of Interest

The authors declare no conflicts of interests.

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Figure 1. The locations of sample collection for S. japonicus. SJB: Boryeong; SJG: Geomundo; SJK: Kangrung.
Figure 1. The locations of sample collection for S. japonicus. SJB: Boryeong; SJG: Geomundo; SJK: Kangrung.
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Figure 2. Neighbor-joining (NJ) tree for control region haplotypes of S. japonicus. Bootstrap supports more than 40% in 1000 replicates are shown. Bar indicates genetic distance. Letters represent geographical distribution of each haplotype. The different colors indicate different populations. SA: S. australasicus is represented as an outgroup.
Figure 2. Neighbor-joining (NJ) tree for control region haplotypes of S. japonicus. Bootstrap supports more than 40% in 1000 replicates are shown. Bar indicates genetic distance. Letters represent geographical distribution of each haplotype. The different colors indicate different populations. SA: S. australasicus is represented as an outgroup.
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Figure 3. Haplotype network based on haplotypes of S. japonicus mtDNA control region. SJB: Boryeong, SJG: Geomundo, SJK: Kangrung. Circle sizes indicate the frequencies of each haplotype. Each short line, perpendicular line connecting haplotypes, represents one mutational step. Circles with abbreviated symbols representing populations.
Figure 3. Haplotype network based on haplotypes of S. japonicus mtDNA control region. SJB: Boryeong, SJG: Geomundo, SJK: Kangrung. Circle sizes indicate the frequencies of each haplotype. Each short line, perpendicular line connecting haplotypes, represents one mutational step. Circles with abbreviated symbols representing populations.
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Figure 4. Mismatch distribution for two clades of S. japonicus. The observed distribution is shown by bars, and the expected distribution under the sudden expansion model based on the sequence of the mtDNA control region is shown by solid lines.
Figure 4. Mismatch distribution for two clades of S. japonicus. The observed distribution is shown by bars, and the expected distribution under the sudden expansion model based on the sequence of the mtDNA control region is shown by solid lines.
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Table 1. Summary of sample collection and the results of genetic analysis in S. japonicus.
Table 1. Summary of sample collection and the results of genetic analysis in S. japonicus.
ZoneLocations (Abbreviation)Collection DateNTL (SD)NhSh (SD)π (SD)
West Sea Boryeong (SJB)12 May 20133225.3 (5.2)18200.948 (0.023)0.012 (0.007)
South Sea Geomundo (SJG)29 May 20133227.2 (6.3)27200.986 (0.012)0.016 (0.008)
East SeaKangrung (SJK)12 April 20133225.9 (5.9)28170.990 (0.010)0.016 (0.008)
Clade 1--61 40220.972 (0.011)0.011 (0.006)
Clade 2--35 26220.980 (0.013)0.008 (0.004)
N: number of samples; Nh: number of haplotypes; S: polymorphic sites; h: haplotype diversity; π: nucleotide diversity; SD: standard deviation.
Table 2. Distribution of different haplotypes belonging to two different clades.
Table 2. Distribution of different haplotypes belonging to two different clades.
Clade 1
HaplotypeSJGSJKSJBHaplotypeSJGSJKSJB
SJG004100SJB019001
SJG005100SJB025001
SJG006100SJB027003
SJG007200SJB028102
SJG008100SJB029001
SJG009100SJB032126
SJG010100Clade 2
SJG012100HaplotypeSJGSJKSJB
SJG013100SJG019200
SJG015100SJG023100
SJG016100SJG024100
SJG017100SJG026100
SJG020100SJG028100
SJG022200SJG029100
SJG025300SJK004010
SJG030100SJK006010
SJG031100SJK008010
SJG032100SJK009020
SJK001010SJK011010
SJK007010SJK013010
SJK012010SJK016010
SJK015010SJK018010
SJK019010SJK025010
SJK021010SJK028010
SJK022020SJK032010
SJK023010SJB002002
SJK024010SJB003001
SJK026010SJB005001
SJK027010SJB015001
SJK029010SJB018001
SJK030010SJB020001
SJB006001SJB021113
SJB010001SJB024012
SJB017023SJB030001
Table 3. Neutrality test and mismatch distribution for S. japonicus.
Table 3. Neutrality test and mismatch distribution for S. japonicus.
Neutrality TestMismatch Distribution
LocationTajima’s DFu’s FsSSDHriτ
SJB0.189−7.020 *0.0110.0207.863
SJG1.234−16.209 *0.0070.0267.080
SJK2.144−18.172 *0.0090.0146.451
Clade 1−0.104−25.593 *0.0010.0135.314
Clade 2−1.285−25.593 *0.0030.0363.361
SSD: sum of squared deviations; Hri: Harpending raggedness index; τ: Time since expansion expressed in units of mutational time; *: Starmark indicates significant value (p < 0.05).
Table 4. Pairwise FST (below diagonal) and associated p values (above diagonal) among three sample locations for the mtDNA control region of S. japonicus.
Table 4. Pairwise FST (below diagonal) and associated p values (above diagonal) among three sample locations for the mtDNA control region of S. japonicus.
LocationSJBSJGSJK
SJB 0.0080.029
SJG0.075 0.007
SJK0.0530.058
Bold numbers indicate significance level (p < 0.05).
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Gwak, W.-S. Population Genetic Structure with Mitochondrial DNA of the Chub Mackerel Scomber japonicus in Korean Coastal Waters. J. Mar. Sci. Eng. 2025, 13, 252. https://doi.org/10.3390/jmse13020252

AMA Style

Gwak W-S. Population Genetic Structure with Mitochondrial DNA of the Chub Mackerel Scomber japonicus in Korean Coastal Waters. Journal of Marine Science and Engineering. 2025; 13(2):252. https://doi.org/10.3390/jmse13020252

Chicago/Turabian Style

Gwak, Woo-Seok. 2025. "Population Genetic Structure with Mitochondrial DNA of the Chub Mackerel Scomber japonicus in Korean Coastal Waters" Journal of Marine Science and Engineering 13, no. 2: 252. https://doi.org/10.3390/jmse13020252

APA Style

Gwak, W.-S. (2025). Population Genetic Structure with Mitochondrial DNA of the Chub Mackerel Scomber japonicus in Korean Coastal Waters. Journal of Marine Science and Engineering, 13(2), 252. https://doi.org/10.3390/jmse13020252

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