Next Article in Journal
Similarity of Microplastic Characteristics between Amphibian Larvae and Their Aquatic Environment
Previous Article in Journal
Long-Term Effects of Pre-Weaning Individual or Pair Housing of Dairy Heifer Calves on Subsequent Growth and Feed Efficiency
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Animals
Volume 14
Issue 5
10.3390/ani14050718
animals-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

Analysis of Genetic Diversity and Structure of Eight Populations of Nerita yoldii along the Coast of China Based on Mitochondrial COI Gene

by
Senping Jiang
1,
Zhenhua Li
2,
Jiji Li
1,
Kaida Xu
2,* and
Yingying Ye
1,*
1
National Engineering Research Center for Marine Aquaculture, Zhejiang Ocean University, Zhoushan 316022, China
2
Key Laboratory of Sustainable Utilization of Technology Research for Fisheries Resources of Zhejiang Province, Scientific Observing and Experimental Station of Fishery Resources for Key Fishing Grounds, Ministry of Agriculture and Rural Affairs of China, Zhejiang Marine Fisheries Research Institute, Zhoushan 316021, China
*
Authors to whom correspondence should be addressed.
Animals 2024, 14(5), 718; https://doi.org/10.3390/ani14050718
Submission received: 31 October 2023 / Revised: 14 January 2024 / Accepted: 29 January 2024 / Published: 25 February 2024
(This article belongs to the Section Animal Genetics and Genomics)
Browse Figures
Versions Notes

Abstract

:

Simple Summary

The mitochondrial COI gene as a molecular marker is widely used in genetic diversity and population genetic diversity analysis. In this study, mitochondrial COI was used to analyze the genetic diversities of eight populations of Nerita yoldii along the coast of China. The results showed that N. yoldii has a high level of genetic diversity, with genetic structure differences observed between the Xiapu population and six other populations, excluding the Taizhou population. The results of neutral tests and nucleotide mismatch analyses indicate a historical demographic expansion in the N. yoldii population. Our study results provide foundational data for the conservation and sustainable utilization of N. yoldii resources.

Abstract

Nerita yoldii is a euryhaline species commonly found in the intertidal zone. To investigate the genetic diversity of 233 N. yoldii individuals from eight locations along the coast of China, we utilized the mitochondrial COI gene as a molecular marker. A total of 34 haplotypes were detected, exhibiting a mean haplotype diversity (Hd) of 0.5915 and a mean nucleotide diversity (Pi) of 0.0025, indicating high levels of genetic diversity among all populations. An analysis of molecular variance (AMOVA) indicated that the primary source of genetic variation occurs within populations. In addition, neutral tests and mismatch analyses suggested that N. yoldii populations may have experienced bottleneck events. Moderate genetic differentiation was observed between Xiapu and other populations, excluding the Taizhou population, and may be attributed to the ocean currents. Intensively studying the genetic variation and population structure of N. yoldii populations contributes to understanding the current population genetics of N. yoldii in the coastal regions of China. This not only provides a reference for the study of other organisms in the same region but also lays the foundation for the systematic evolution of the Neritidae family.

1. Introduction

The family Neritidae comprises more than 300 species and is recognized for its remarkable diversity and extensive geographical distribution. Fossil evidence suggests that their ancestors inhabited the late Cretaceous period [1]. The adaptability of these gastropods to different salinity levels and habitats makes them a widely distributed group that thrives in brackish, marine, and freshwater ecosystems. They mainly inhabit tropical to subtropical regions, with only a few species found in temperate regions [2], such as Nerita atramentosa, primarily distributed in the temperate regions of southern Queensland (eastern) and western Australia [3], and the Japanese species Neritilia mimotoi, which inhabits the warm temperate region [2]. A previous study shed light on the factors contributing to the broad salinity tolerance of Neritidae species, which can be attributed to their recurrent colonization of marine, brackish, and freshwater environments throughout their evolutionary history [4]. The life history of most species in the Neritidae family is not well-documented, but it is established that most of them undergo a relatively prolonged planktonic phase.
Belonging to the family Neritidae, Nerita yoldii Récluz 1841 exhibits an overall semi-oval shape, characterized by a row of fine teeth on the inner edge of the outer lip and two to three teeth in the center of the inner lip. Although its appearance is described in detail, it is difficult to distinguish it from other species in the family of Neritidae based on morphological characteristics alone. For example, due to the similar morphological characteristics, Tsuchiya (2017) [5] regards N. yoldii to be a synonym of Nerita squamulata Le Guillou, 1841 in a 2000 study. With the advancement of molecular biology techniques, molecular markers have become a commonly used auxiliary method for species identification, aiding in the differentiation of other species within the Neritidae family. In China, predominantly inhabiting the coastal regions south of Zhejiang Province in the 1960s [6], N. yoldii thrives in the intertidal reef hard-bottom areas. Temperature plays a pivotal role in shaping the distribution of N. yoldii. However, recent studies have detected signs of its presence beyond Zhejiang Province, specifically in areas north of the province, such as Jiangsu Province. The migration of N. yoldii across the Yangtze River barrier into the more northern Jiangsu Province is believed to be a consequence of climate change, particularly global warming and rising temperatures, alongside human activities. The spawning period of N. yoldii in China was April–August, and the pelagic larvae of N. yoldii from the pristine marginal seas south of the Yangtze River also provide the potential for it to overcome the Yangtze River barrier and contribute to genetic variation among populations [7,8].
Avise (2000) [9] and Hewitt (2000) [10] mentioned that the distribution and genetic structure of the marine animals were closely related to historical climatic changes in the sea level, water temperature, and ocean currents. Compared to terrestrial species, marine animals are generally considered to have no obvious genetic structure and low genetic diversity. Especially in some Mollusca with a planktonic period, their plankton, larval or adult, could be transmitted with the ocean current and usually do not have many physical barriers to movement [11]. Planktonic larvae spread with the ocean currents and influence genetic structure by facilitating the exchanges of gene flow within populations [12]. The length of the planktonic larvae also is a significant factor in their distribution and genetic structure, and longer planktonic larval durations confer greater dispersal ability [13,14,15]. For example, Ye (2018) [16] used the COI gene to explore the genetic diversity and genetic structure of the clam Gomphina aequilatera in China and found that the distribution and genetic structure of G. aequilatera were related to the ocean current; the study concluded that species with a short planktonic larval stage have a strong population structure.
Mitochondrial cytochrome coxidase (COX) is an important component of the fourth protein complex in the mitochondrial respiratory chain, and it plays a significant role in various physiological activities, especially in energy supply, apoptosis, and metabolism [17]. The mitochondrial COI gene has advantages, including high conservatism, a low mutation rate, and maternal inheritance [18,19,20]. Consequently, it has emerged as a widely utilized molecular marker in genetic studies of almost all groups of animals, protists, and plants, especially for investigating phylogeny and genealogical geography [21,22,23,24,25,26,27]. It also has been widely used in Mollusca, such as Ruditapes philippinarum [28], Haliotis diversicolor [29], freshwater mussels [30], and so on.
In this study, we focused on examining the genetic diversity, genetic structure, and population history dynamics of N. yoldii along the coast of China, utilizing the mitochondrial COI gene. Our objectives were to characterize the genetic diversity of N. yoldii within and between populations. The results from this study may provide some support for using the germplasm resources and maintaining the genetic resources of N. yoldii.

2. Materials and Methods

2.1. Experimental Animals and Sampling

According to the N. yoldii geographical distribution along the coast of China, we randomly selected eight sites from the coast of China and collected a total of 233 individuals (Shengsi [SS], Liuheng [LH], Xiangshan [XM], Taizhou [TZ], Fuding [FD], Xiapu [XP], Xiamen (XM), Shantou [ST]) along the coast of China (Figure 1, Table 1). All experimental samples were approved by the State Oceanic Administration of China and the Ethics Committee of Zhejiang Ocean University and were performed according to national laws and regulations. The total samples were identified, and their muscle tissues were collected and saved in absolute alcohol at −20 °C.

2.2. DNA Extraction and Polymerase Chain Reaction Amplification

The genomic DNA of each sample was extracted by a salt-extraction procedure [31] and measured on a 1.5% agarose gel, then stored in a −20 °C freezer for later use. Based on the complete mitochondrial genome (MK395169) of N. yoldii, primers were designed using Primer Premier 5.0 software (Premier Biosoft International, San Franciso, CA, USA). The forward primers and reverse primers were 5′-GCACTAAGTGAGTCCTTGTTAAAT-3′ (COI-F) and 5′-ATTGATAGCCAAATCAAATTGTAAC-3′ (COI-R), respectively. The PCR reactions were performed in a total volume of 25 μL, comprising 12.5 μL of Taq MasterMix (Beijing Com Win Biotech Co., Ltd., Beijing, China), 1 μL of forward primer, 1 μL of reverse primer, 1 μL of genomic DNA, and 10 μL of ddH2O. The PCR amplification procedure was predenaturation at 95 °C for 3 min, then denaturation at 95 °C for 30 s, annealing at 49 °C for 30 s, 72 °C for 1 min for 30 cycles, and finally 72 °C for 10 min. The amplification products were detected and observed with the 1.5% agarose gel and sent to TSINGKE Biotech Co., Ltd. (Hangzhou, China) for bidirectional sequencing.

2.3. Data Analysis

The sequencing results were analyzed with BioEdit v7.2.6.1 software, and the fragments with standard peak type and no interference were screened and made into FASTA files with Microsoft Excel 2016 (MSO, Version 2312. The COI sequences of all sequenced N. yoldii individuals were serially compared using the BLAST tool in the NCBI database (URL: https://blast.ncbi.nlm.nih.gov/Blast.cgi, accessed on 21 May 2023) to confirm the species attribution of the sample, and individuals with a comparison similarity of less than 99% were eliminated and saved as FASTA files. MEGA-X software [32] was used to compare sequences and cut the ends flat. Then, DnaSP 6 software [33] was used to distinguish haplotypes and count the classical genetic parameters, such as haplotype diversity (h), nucleotide diversity (Pi), etc. It was also used in a mismatch analysis. An analysis of molecular variance (AMOVA), a genetic differentiation index (FST), and a neutrality test between two populations were performed with Arlequin v3.5.2.2 software [34]. Network 10.2.0.0 software [35] was used to build a haplotype network diagram, and a phylogenetic tree was built with the final MEGA-X software. Gene flow network diagrams were constructed using divMigrate-online software [36].

3. Results

3.1. Characteristics of the COI Sequence and the Genetic Diversity of N. yoldii

The total length of the COI gene after comparison shearing was 494 bp, which was amplified from 233 individuals of N. yoldii. The average nucleotide frequencies among all sequences were 41.8% T, 14.2% C, 23.1% A, and 20.9% G, respectively. The A/T content (64.9%) was significantly higher than the C/G content (35.1%). Only 34 variable sites were found. Genetic diversity within the N. yoldii populations along the coast of China was investigated by analyzing the mitochondrial COI sequences (Table 2). Haplotype analysis showed a total of 34 haplotypes across the eight populations. Among the 233 COI sequences examined, haplotype numbers (h) ranged from 4 (LH) to 12 (ST). In this study, the haplotype diversity (Hd) across the eight populations exhibited a wide range, spanning from 0.2292 to 0.7536, with the majority of the populations displaying a pronounced high level of haplotype diversity (Hd > 0.5). Notably, the LH population stood out as an exception, demonstrating relatively lower haplotype diversity (Hd < 0.5). The nucleotide diversity (Pi) ranged from 0.0008 to 0.0037 across the eight populations, with all population exhibiting low levels of nucleotide diversity (Pi) (Pi < 0.005). Additionally, the average nucleotide difference (K) concurred with the nucleotide diversity (Pi), revealing minimal population-level differentiation.

3.2. Population Genetic Structure of N. yoldii

Genetic distances within populations ranged 0.0008 to 0.0037, while distances between populations ranged 0.0014 to 0.0036. The results of the molecular variance analysis (AMOVA) across the eight N. yoldii populations indicated that the primary genetic variations occurred within populations, representing 96.62% of the total variation. Contrary to the assumption of low levels of genetic variation among populations (3.38%), a significant portion of the variation was observed within populations (Table 3). The results of the pairwise FST values between populations ranged from −0.0002 to 0.1523. While most results indicated no differentiations and lacked significance, medium levels of differentiation (0.05 < FST < 0.25) were observed between the XP population and the other populations, except for the TZ population (Figure 2). Additionally, significant differentiations were evident between the XP population and the other four populations (SS, LH, XS, and ST). Migration dynamic analysis (Figure 3) revealed varying degrees of gene exchanges among different populations. The gene flow (Figure 2) confirmed a degree of genetic differentiation among populations. Furthermore, the gene flow between the XP population and the other populations was weak, except for the TZ population. The haplotype network illustrated a lack of significant differentiation among the 34 haplotypes in the eight populations along the Chinese coast, with XP population haplotypes concentrated on the right (Figure 4). Notably, haplotype 1 was located at the center, closely related to most other haplotypes, suggesting its ancestral nature within these N. yoldii populations. Conversely, haplotype 19 branched off separately, with most haplotypes within this branch distributed among the XP, XM, and ST populations. The phylogenetic tree constructed through the neighbor-joining analysis (Figure 5) revealed a close relationship between the XM and ST populations. Similarly, the LH population showed close proximity to the SS population. The XP population was closely related to the TZ population but distantly related to several other populations.

3.3. Population Phylogenetic Analysis

In the Tajima’s D test, the test value of each population was found to be negative and significantly deviated from neutrality, except for the XS, TZ, and XP populations. Similar trends were observed in the Fu’s FS test, with the test value of each population displaying significant negative deviation from neutrality, except for the LH, TZ, and XP populations (Table 4). The results from both the Tajima’s D test and the Fu’s FS test suggest that N. yoldii might have been subjected to negative selection or bottleneck amplification during its evolutionary history. The mismatch analysis yielded results that differed from the observed values, indicating a unimodal Poisson distribution that closely resembled the expected curve, thus pointing towards an expansion effect within the population (Figure 6). By utilizing the mitochondrial evolution rate of the N. yoldii populations, it was estimated that the expansion of the cockle population occurred approximately during the Pleistocene.

4. Discussion

4.1. Genetic Diversity of the Eight Populations of N. yoldii along the Coast of China

Genetic diversity plays a crucial role in biological evolution as richer genetic diversity allows for greater adaptability to the environment and facilitates increased survivability. Grant (1998) [37] classified haplotype diversity levels and nucleotide diversity levels, considering haplotype diversity greater than 0.5 as high and vice versa. Similarly, nucleotide diversity greater than 0.005 is considered high and vice versa. Conversely, diminished genetic diversity often results in vulnerability to bottleneck effects and other factors that can lead to population decline. In the present study, the eight populations from the coast of China were marked by the COI gene. The mean Hd of these populations was 0.5915, indicating a high state, while the mean Hd was 1.2548 and the mean Pi was 0.0025, signifying a comparatively low state. The results of the mean Hd and Pi were similar to Thais clavigera, which was also analyzed using the COI gene. The mean Hd of the nine populations of T. clavigera distributed along the coast of China was 0.69826, slightly higher than the N. yoldii populations, and the mean Pi was 0.00182, slightly lower than the N. yoldii populations. However, both exhibited high levels of haplotype diversity and low levels of nucleotide diversity [38]. This situation can be interpreted as a bottleneck effect. The characteristics of a population undergoing a bottleneck include a significant reduction in population size at a specific period, leading to a small effective population size and a decline in genetic diversity. Subsequently, there is a rapid population expansion, facilitating the retention of new mutations and resulting in a recovery of genetic diversity [9,39]. Feng et al. (2021) [40] estimated that the divergence of N. yoldii occurred approximately 16.89 Mya, during the Neogene. This suggests that N. yoldii may have experienced the Quaternary glaciations. The East China Sea, situated in the western Pacific, had one of the most extensive shelves globally, exposing a total area of 850,000 km2 during the Pleistocene ice ages [41]. In this environmental context, the habitat of N. yoldii was constrained, leading to a sharp decline in population size, a reduction in effective population size, and a decrease in genetic diversity. As the Ice Age concluded, the habitat of N. yoldii recovered, and its population underwent rapid growth, promoting the retention of new mutations. Consequently, N. yoldii exhibited a condition of high haplotype diversity and low nucleotide diversity, a pattern observed in many marine invertebrates [42,43].

4.2. Population Differentiation of the Eight Populations of N. yoldii along the Coast of China

The measurement of FST is critical in determining population differentiation in genetic studies. An FST value ranging from 0 to 0.05 indicates no differentiation, 0.05 to 0.15 signifies a low level of differentiation, 0.15 to 0.25 suggests a medium level of differentiation, and values exceeding 0.25 imply a significant degree of differentiation [44]. In this study, the FST value of the XP population and the other populations ranged from 0.05 to 0.15, except for the TZ population, with a significance level of p < 0.05, except for the TZ, FD, XP, and XM populations. These findings suggest a noticeable differentiation between the XP population and all the other populations, excluding the TZ population. We postulate that these differences may be associated with the Kuroshio Current and coastal currents [43,45]. Some marine organisms commonly show reduced genetic differentiation across extensive spatial ranges, displaying limited genetic structure. This phenomenon is often linked to the presence of a planktonic phase in many marine invertebrates, during which larvae disperse via ocean currents. This widespread dispersal mechanism facilitates gene flow among diverse geographic populations, contributing to lower levels of genetic differentiation and the manifestation of genetic homogeneity [46].
Originating between 12 and 15 degrees north latitude around the Philippines, the Kuroshio Current enters the East China Sea through the East Taiwan Channel, situated between the northeast of Taiwan and Yonaguni-Jima Island at the southwestern tip of the Ryukyu Islands. Additionally, smaller portions of the Kuroshio intrude into the East China Sea shelf through the Luzon and Taiwan Straits [47]. In addition, the coastal current is a main reason for the population differentiation. Especially, observations by Yuan and Li suggest a prominent southwestward stream of shelf water across the East China Sea that is discernible from the distribution of fine-grained sediments [48,49]. In all coastal currents, the Zhejiang–Fujian current exhibits distinct seasonal characteristics [50]. During the winter, under the action of northerly winds, the Yangtze River rushes southward along the Zhejiang coast to the Fujian coast, while in the summer, it flows northward along the coast [51]. Simultaneously, under the influence of robust northeast winds, the East Guangdong Sea Current travels southwest, intersecting with the Fujian and Zhejiang Sea Currents. In the summer, the East Guangdong Sea Current flows northeast, entering the Taiwan Strait [52,53]. Similar to many Mollusca [12], N. yoldii feature a planktonic phase. During this period, guided by ocean currents, frequent gene exchanges between populations occur, potentially accounting for the phenomenon of the N. yoldii differentiation.

4.3. Phylogeny of the Eight Populations of N. yoldii along the Coast of China

The phylogeny of the eight populations of N. yoldii along the coast of China is strongly influenced by the significant role of the China Southeast Sea as a key component of the northwest Pacific, representing a vital marine center of origin [54]. This sea is delineated into two marginal seas, the East China Sea and the South China Sea, separated by the Taiwan Strait. During the glacial epoch, the drop in sea levels facilitated the connection of the Taiwan Strait with the shelf of the East China Sea, leading to the physical segregation of the East China Sea and the South China Sea. Conversely, during the interglacial periods, the rise in sea levels caused the Taiwan Strait to disconnect from the shelf of the East China Sea, enabling the interconnection between the East China Sea and the South China Sea [54,55,56]. These geological phenomena provided the potential for historical population demographic expansion in the marine environment. The findings derived from the neutral tests and mismatch analyses conducted on N. yoldii substantiate the idea that similar evolutionary processes have shaped its genetic history. We estimated the population expansion time using the formula t = τ/(2μk), where τ represents the parameter in the sudden expansion model, k denotes the sequence length in our study, and μ is the mutation rate across the entire sequence [57]. Unfortunately, we could not determine a precise value for μ, so we conducted a simple estimation of the expansion time. The estimated expansion time falls approximately within the Pleistocene epoch [58]. This observation lends additional support to the notion that N. yoldii may have experienced the geological events mentioned earlier. It is speculated that N. yoldii may come from the same ancestral group from shelters in the East China Sea during the glacial period towards the end of the Pleistocene epoch. Additionally, the features presented by the haplotype network also corroborate this point. In this network, individual haplotypes primarily accumulate through gradual base mutations from the ancestral haplotype, showing an overall lack of distinct branches, with the majority of haplotypes clustering around the central ancestral haplotype.

5. Conclusions

This research utilized the mtDNA COI gene as a molecular marker to investigate the genetic diversity and structure of eight N. yoldii populations along the coast of China. The investigation revealed a substantial presence of high levels of genetic diversity and low levels of nucleotide diversity of N. yoldii. Generally, no significant genetic structures were observed, except for the XP population, which displayed marked and moderate genetic differentiation. The exception was the TZ population, possibly influenced by the Kuroshio Current and coastal currents. These findings enhance our understanding of the genetic diversities of N. yoldii and provide reference data for the rational and effective utilization of and research on the family Neritidae. Unfortunately, samples from the northernmost region (north of the Yangtze River) failed to be collected. Further research is needed to investigate whether the observed northward migration has genetic implications.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/ani14050718/s1, Table S1: The 34 haplotypes distribution of eight N. yoldii populations based on COI gene.; Table S2: Genetic distance of eight N. yoldii populations based on COI gene.

Author Contributions

Conceptualization, S.J.; methodology, S.J. and Z.L.; software, S.J.; validation, K.X. and Y.Y.; formal analysis, S.J.; resources, S.J.; data curation, S.J.; writing—original draft preparation, S.J., Z.L., and J.L.; writing—review and editing, Y.Y. and K.X.; funding acquisition, J.L. and Y.Y. All authors have read and agreed to the published version of the manuscript.

Funding

The present manuscript was financially supported by the Project of Bureau of Science and Technology of Zhoushan (No. 2021C21017) and the National Key R&D Program of China (2019YFD0901204).

Institutional Review Board Statement

All animal experiments were conducted under the guidance of and approved by the Animal Research and Ethics Committee of Zhejiang Ocean University. Approval code: 2023087, Approval date: 8 May 2023.

Informed Consent Statement

Informed consent was obtained from all subjects involved in this study.

Data Availability Statement

Data are contained within the article and Supplementary Materials.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Kano, Y.; Chiba, S.; Kase, T. Major adaptive radiation in neritopsine gastropods estimated from 28S rRNA sequences and fossil records. Proc. Biol. Sci. 2002, 269, 2457–2465. [Google Scholar] [CrossRef]
  2. Sasaki, T.; Ishikawa, H. The first occurrence of a neritopsine gastropod from a phreatic community. J. Molluscan Stud. 2002, 68, 286–288. [Google Scholar] [CrossRef]
  3. Waters, J.M.; King, T.M.; O’Loughlin, P.M.; Spencer, H.G. Phylogeographical disjunction in abundant high-dispersal littoral gastropods. Mol. Ecol. 2005, 14, 2789–2802. [Google Scholar] [CrossRef]
  4. Qi, L.; Xu, B.; Kong, L.; Li, Q. Improved phylogenetic resolution within Neritidae (Gastropoda, Nertimorpha) with implications for the evolution of shell traits and habitat. Zool. Scr. 2023, 52, 46–57. [Google Scholar] [CrossRef]
  5. Okutani, T. Marine Mollusks in Japan, 2nd ed.; Okutani, T., Ed.; Tokai University Press: Shibuya, Japan, 2017; pp. 259–1292. [Google Scholar]
  6. Zhang, X.; Qi, Z.; Zhang, F.; Ma, X. A preliminary study of the demarcation of marine Molluscan faunal regions of China and its adjacent waters. Oceanol. Limnol. Sin. 1963, 5, 124–138. [Google Scholar]
  7. Jie, W.; Yan, H.Y.; Cheng, Z.Y.; Huang, X.W.; Wei, W.; Ding, M.W.; Dong, Y.W. Recent northward range extension of Nerita yoldii (Gastropoda: Neritidae) on artificial rocky shores in China. J. Molluscan Stud. 2018, 84, 345–353. [Google Scholar]
  8. Wang, J.; Cheng, Z.Y.; Dong, Y.W. Demographic, physiological and genetic factors linked to the poleward range expansion of the snail Nerita yoldii along the shoreline of China. Mol. Ecol. 2022, 31, 4510–4526. [Google Scholar] [CrossRef] [PubMed]
  9. Avise, J.C. Phylogeography: The History and Formation of Species; Harvard University Press: Cambridge, MA, USA, 2000. [Google Scholar]
  10. Hewitt, G. The genetic legacy of the Quaternary ice ages. Nature 2000, 405, 907–913. [Google Scholar] [CrossRef] [PubMed]
  11. Liu, H.; Liu, M.; Ge, S.; Wang, Q.; Yu, D.; Guan, S. Population structuring and historical demography of a common clam worm Perinereris aibuhitensis near the coasts of Shandong Peninsula. Biochem. Syst. Ecol. 2012, 44, 70–78. [Google Scholar] [CrossRef]
  12. Gary, S.F.; Fox, A.D.; Biastoch, A.; Roberts, J.M.; Cunningham, S.A. Larval behaviour, dispersal and population connectivity in the deep sea. Sci. Rep. 2020, 10, 10675. [Google Scholar] [CrossRef]
  13. Woodson, C.B.; McManus, M.A. Foraging behavior can influence dispersal of marine organisms. Limnol. Oceanogr. 2007, 52, 2701–2709. [Google Scholar] [CrossRef]
  14. Toonen, R.; Pawlik, J.R. Settlement of the gregarious tube worm Hydroides dianthus (Polychaeta: Serpulidae). I. Gregarious and nongregarious settlement. Mar. Ecol. Prog. Ser. 2001, 224, 103–114. [Google Scholar] [CrossRef]
  15. Addison, J.A.; Hart, M.W. Analysis of population genetic structure of the green sea urchin (Strongylocentrotus droebachiensis) using microsatellites. Mar. Biol. 2004, 144, 243–251. [Google Scholar] [CrossRef]
  16. Ye, Y.; Fu, Z.; Tian, Y.; Li, J.; Guo, B.; Lv, Z.; Wu, C. Pelagic larval dispersal habits influence the population genetic structure of clam Gomphina aequilatera in China. Genes Genom. 2018, 40, 1213–1223. [Google Scholar] [CrossRef] [PubMed]
  17. Timón-Gómez, A.; Nývltová, E.; Abriata, L.A.; Vila, A.J.; Hosler, J.; Barrientos, A. Mitochondrial cytochrome c oxidase biogenesis: Recent developments. Semin. Cell Dev. Biol. 2018, 76, 163–178. [Google Scholar] [CrossRef]
  18. Jiang, L.; Kang, L.; Wu, C.; Chen, M.; Lü, Z. A comprehensive description and evolutionary analysis of 9 Loliginidae mitochondrial genomes. Hydrobiologia 2018, 808, 115–124. [Google Scholar] [CrossRef]
  19. Dai, L.; Kausar, S.; Abbas, M.N.; Wang, T.-T. Complete sequence and characterization of the Ectropis oblique mitochondrial genome and its phylogenetic implications. Int. J. Biol. Macromol. 2018, 107 Pt A, 1142–1150. [Google Scholar] [CrossRef]
  20. Feng, J.; Guo, Y.; Yan, C.; Ye, Y.; Li, J.; Guo, B.; Lü, Z. Sequence comparison of the mitochondrial genomes in two species of the genus Nerita (Gastropoda: Neritimorpha: Neritidae): Phylogenetic implications and divergence time estimation for Neritimorpha. Mol. Biol. Rep. 2020, 47, 7903–7916. [Google Scholar] [CrossRef]
  21. Devassy, A.; Kumar, R.; Shajitha, P.P.; John, R.; Padmakumar, K.G.; Basheer, V.S.; Gopalakrishnan, A.; Mathew, L. Genetic identification and phylogenetic relationships of Indian clariids based on mitochondrial COI sequences. Mitochondrial DNA Part A DNA Mapp. Seq. Anal. 2016, 27, 3777–3780. [Google Scholar] [CrossRef]
  22. Toda, S.; Osakabe, M.; Komazaki, S. Interspecific diversity of mitochondrial COI sequences in Japanese Panonychus species (Acari: Tetranychidae). Exp. Appl. Acarol. 2000, 24, 821–829. [Google Scholar] [CrossRef]
  23. Dumidae, A.; Janthu, P.; Subkrasae, C.; Pumidonming, W.; Dekumyoy, P.; Thanwisai, A.; Vitta, A. Genetic analysis of Cryptozona siamensis (Stylommatophora, Ariophantidae) populations in Thailand using the mitochondrial 16S rRNA and COI sequences. PLoS ONE 2020, 15, e0239264. [Google Scholar] [CrossRef]
  24. Wang, W.; Zhang, K.; Deng, D.; Zhang, Y.N.; Peng, S.; Xu, X. Genetic Diversity of Daphnia pulex in the Middle and Lower Reaches of the Yangtze River. PLoS ONE 2016, 11, e0152436. [Google Scholar] [CrossRef]
  25. Li, X.; Zhang, Z.; Zhang, J.; Huang, J.; Wang, L.; Li, Y.; Hafeez, M.; Lu, Y. Population Genetic Diversity and Structure of Thrips tabaci (Thysanoptera: Thripidae) on Allium Hosts in China, Inferred From Mitochondrial COI Gene Sequences. J. Econ. Entomol. 2020, 113, 1426–1435. [Google Scholar] [CrossRef]
  26. Qasim, M.; Baohua, W.; Zou, H.; Lin, Y.; Dash, C.K.; Bamisile, B.S.; Hussain, M.; Zhiwen, Z.; Wang, L. Phylogenetic relationship and genetic diversity of citrus psyllid populations from China and Pakistan and their associated Candidatus bacterium. Mol. Phylogenet. Evol. 2018, 126, 173–180. [Google Scholar] [CrossRef]
  27. Woolley, V.C.; Tembo, Y.L.; Ndakidemi, B.; Obanyi, J.N.; Arnold, S.E.; Belmain, S.R.; Ndakidemi, P.A.; Ogendo, J.O.; Stevenson, P.C. The diversity of aphid parasitoids in East Africa and implications for biological control. Pest Manag. Sci. 2022, 78, 1109–1116. [Google Scholar] [CrossRef]
  28. Mao, Y.; Gao, T.; Yanagimoto, T.; Xiao, Y. Molecular phylogeography of Ruditapes philippinarum in the Northwestern Pacific Ocean based on COI gene. J. Exp. Mar. Biol. Ecol. 2011, 407, 171–181. [Google Scholar] [CrossRef]
  29. Hsu, T.-H.; Gwo, J.-C. Genetic diversity and stock identification of small abalone (Haliotis diversicolor) in Taiwan and Japan. PLoS ONE 2017, 12, e0179818. [Google Scholar] [CrossRef]
  30. Huang, X.C.; Su, J.H.; Ouyang, J.X.; Ouyang, S.; Zhou, C.H.; Wu, X.P. Towards a global phylogeny of freshwater mussels (Bivalvia: Unionida): Species delimitation of Chinese taxa, mitochondrial phylogenomics, and diversification patterns. Mol. Phylogenet. Evol. 2019, 130, 45–59. [Google Scholar] [CrossRef]
  31. Aljanabi, S.M.; Martinez, I. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res. 1997, 25, 4692–4693. [Google Scholar] [CrossRef]
  32. Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef] [PubMed]
  33. Rozas, J.; Ferrer-Mata, A.; Sánchez-DelBarrio, J.C.; Guirao-Rico, S.; Librado, P.; Ramos-Onsins, S.E.; Sánchez-Gracia, A. DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. Mol. Biol. Evol. 2017, 34, 3299–3302. [Google Scholar] [CrossRef]
  34. Excoffier, L.; Lischer, H.E. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 2010, 10, 564–567. [Google Scholar] [CrossRef]
  35. Bandelt, H.J.; Forster, P.; Röhl, A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 1999, 16, 37–48. [Google Scholar] [CrossRef]
  36. Sundqvist, L.; Keenan, K.; Zackrisson, M.; Prodöhl, P.; Kleinhans, D. Directional genetic differentiation and relative migration. Ecol. Evol. 2016, 6, 3461–3475. [Google Scholar] [CrossRef] [PubMed]
  37. Grant, W.; Bowen, B. Shallow population histories in deep evolutionary lineages of marine fishes: Insights from sardines and anchovies and lessons for conservation. J. Hered. 1998, 89, 415–426. [Google Scholar] [CrossRef]
  38. Yan, C.; Miao, J.; Feng, J.; Xia, L.; Ye, Y.; Li, J.; Guo, B. Pelagic Larval Dispersal Habits Shape the Weak Population Structure of Thais clavigera in the Coastal Areas of China Sea. Pak. J. Zool. 2023. [Google Scholar] [CrossRef]
  39. Rogers, A.R.; Harpending, H. Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 1992, 9, 552–569. [Google Scholar] [PubMed]
  40. Feng, J.T.; Xia, L.P.; Yan, C.R.; Miao, J.; Ye, Y.Y.; Li, J.J.; Guo, B.Y.; Lü, Z.M. Characterization of four mitochondrial genomes of family Neritidae (Gastropoda: Neritimorpha) and insight into its phylogenetic relationships. Sci. Rep. 2021, 11, 11748. [Google Scholar] [CrossRef] [PubMed]
  41. Liu, J.-X.; Gao, T.-X.; Yokogawa, K.; Zhang, Y.-P. Differential population structuring and demographic history of two closely related fish species, Japanese sea bass (Lateolabrax japonicus) and spotted sea bass (Lateolabrax maculatus) in Northwestern Pacific. Mol. Phylogenet. Evol. 2006, 39, 799–811. [Google Scholar] [CrossRef] [PubMed]
  42. Ni, G.; Li, Q.; Kong, L.; Zheng, X. Phylogeography of bivalve Cyclina sinensis: Testing the historical glaciations and Changjiang River outflow hypotheses in northwestern Pacific. PLoS ONE 2012, 7, e49487. [Google Scholar] [CrossRef]
  43. Zhou, N.; Shen, H.; Chen, C.; Sun, B.; Zheng, P.; Wang, C. Genetic structure of Onchidium “struma” (Mollusca: Gastropoda: Eupulmonata) from the coastal area of China based on mtCO I. Mitochondrial DNA Part A DNA Mapp. Seq. Anal. 2016, 27, 1319–1323. [Google Scholar]
  44. Wright, S. Evolution in Mendelian Populations. Genetics 1931, 16, 97–159. [Google Scholar] [CrossRef]
  45. Zhan, A.; Hu, J.; Hu, X.; Zhou, Z.; Hui, M.; Wang, S.; Peng, W.; Wang, M.; Bao, Z. Fine-Scale Population Genetic Structure of Zhikong Scallop (Chlamys farreri): Do Local Marine Currents Drive Geographical Differentiation? Mar. Biotechnol. 2009, 11, 223–235. [Google Scholar] [CrossRef]
  46. Je Lee, H.; Boulding, E.G. Spatial and temporal population genetic structure of four northeastern Pacific littorinid gastropods: The effect of mode of larval development on variation at one mitochondrial and two nuclear DNA markers. Mol. Ecol. 2009, 18, 2165–2184. [Google Scholar] [CrossRef] [PubMed]
  47. Hu, F.; Liu, Y.; Xu, Z.; Yin, Y.; Hou, Y. Bidirectional Volume Exchange between Kuroshio and East China Sea Shelf Water Based on a Whole-Region Passive-Tracing Method. J. Geophys. Res. Oceans 2020, 125, e2019JC015528. [Google Scholar] [CrossRef]
  48. Yuan, D.; Zhu, J.; Li, C.; Hu, D. Cross-shelf circulation in the Yellow and East China Seas indicated by MODIS satellite observations. J. Mar. Syst. 2008, 70, 134–149. [Google Scholar] [CrossRef]
  49. Li, G.; Qiao, L.; Dong, P.; Ma, Y.; Xu, J.; Liu, S.; Liu, Y.; Li, J.; Li, P.; Ding, D.; et al. Hydrodynamic condition and suspended sediment diffusion in the Yellow Sea and East China Sea. J. Geophys. Res. Oceans 2016, 121, 6204–6222. [Google Scholar] [CrossRef]
  50. Jilan, S. Overview of the South China Sea circulation and its influence on the coastal physical oceanography outside the Pearl River Estuary. Cont. Shelf Res. 2004, 24, 1745–1760. [Google Scholar] [CrossRef]
  51. Chen, R.; Li, J. Large-scale ecological study on planktonic ostracoda in China’s seas and adjacent waters Ⅱ. Correlation between planktonic ostracoda and water systems. Acta Oceanol. Sin. (Chin. Ed.) 1998, 20, 96–101. [Google Scholar]
  52. Xue, C.; Zhang, Y. Sediment transportation of longshore current and coastal current in China littoral zone. Mar. Geol. Quat. Geol. 2010, 30, 1–8. [Google Scholar] [CrossRef]
  53. Wu, J.; Chen, J.; Wang, C.; Yan, X.; Yin, X.; Liu, Q. Constraining the origin of sedimentary organic matter in the eastern Guangdong coast of China using δ13C and δ15N. Front. Mar. Sci. 2023, 10, 1234116. [Google Scholar] [CrossRef]
  54. Briggs, J.C. Marine centres of origin as evolutionary engines. J. Biogeogr. 2003, 30, 1–18. [Google Scholar] [CrossRef]
  55. Pinxian, W.; Xiangjun, S. Last glacial maximum in China: Comparison between land and sea. CATENA 1994, 23, 341–353. [Google Scholar] [CrossRef]
  56. Voris, H.K. Maps of Pleistocene sea levels in Southeast Asia: Shorelines, river systems and time durations. J. Biogeogr. 2000, 27, 1153–1167. [Google Scholar] [CrossRef]
  57. Wang, L.; Yu, H.; Li, Q. Development of microsatellite markers and analysis of genetic diversity of Barbatia virescens in the southern coasts of China. Genes Genom. 2019, 41, 407–416. [Google Scholar] [CrossRef]
  58. Marko, P.B. Fossil calibration of molecular clocks and the divergence times of geminate species pairs separated by the isthmus of panama. Mol. Biol. Evol. 2002, 19, 2005–2021. [Google Scholar] [CrossRef]
Animals 14 00718 g001
Figure 1. Picture showing the sampling locations along the coast of China. SS stands for Shengsi, LH stands for Liuheng, XS stands for Xiangshan, TZ stands for Taizhou, FD stands for Fuding, XP stands for Xiapu, XM stands for Xiamen, and ST stands for Shantou.
Figure 1. Picture showing the sampling locations along the coast of China. SS stands for Shengsi, LH stands for Liuheng, XS stands for Xiangshan, TZ stands for Taizhou, FD stands for Fuding, XP stands for Xiapu, XM stands for Xiamen, and ST stands for Shantou.
Animals 14 00718 g001
Animals 14 00718 g002
Figure 2. FST and Nm of eight N. yoldii populations based on COI gene. Separated by the diagonal line, the blue part represents the FST and the red part represents the gene flow, and the darker the color, the greater the value. ‘*’ indicates significance with probability at 0.05, and the FST greater than 0.05 is displayed.
Figure 2. FST and Nm of eight N. yoldii populations based on COI gene. Separated by the diagonal line, the blue part represents the FST and the red part represents the gene flow, and the darker the color, the greater the value. ‘*’ indicates significance with probability at 0.05, and the FST greater than 0.05 is displayed.
Animals 14 00718 g002
Animals 14 00718 g003
Figure 3. Directional relative migration networks of eight N. yoldii populations constructed with divMigrate using Nm values above 0.5.
Figure 3. Directional relative migration networks of eight N. yoldii populations constructed with divMigrate using Nm values above 0.5.
Animals 14 00718 g003
Animals 14 00718 g004
Figure 4. The haplotype network of eight N. yoldii populations based on COI gene. The colors represent the different populations, and the circle size represents the number of haplotypes.
Figure 4. The haplotype network of eight N. yoldii populations based on COI gene. The colors represent the different populations, and the circle size represents the number of haplotypes.
Animals 14 00718 g004
Animals 14 00718 g005
Figure 5. The neighbor-joining phylogenetic tree based on genetic distances of the mitochondrial COI gene of eight N. yoldii populations.
Figure 5. The neighbor-joining phylogenetic tree based on genetic distances of the mitochondrial COI gene of eight N. yoldii populations.
Animals 14 00718 g005
Animals 14 00718 g006
Figure 6. The mismatch analysis of eight N. yoldii populations based on COI gene.
Figure 6. The mismatch analysis of eight N. yoldii populations based on COI gene.
Animals 14 00718 g006
Table 1. The sampling details for eight populations of N. yoldii.
Table 1. The sampling details for eight populations of N. yoldii.
Sampling SiteAbbreviationCoordinatesSampling DateSample Size
ShengsiSS30°44′ N 122°28′ E2023.0332
LiuhengLH29°40′ N 122°12′ E2021.0133
XiangshanXS29°26′ N 121°58′ E2021.0130
TaizhouTZ28°13′ N 121°22′ E2023.0530
FudingFD27°09′ N 120°25′ E2019.0826
XiapuXP26°52′ N 120°04′ E2018.1130
XiamenXM24°26′ N 118°04′ E2021.0424
ShantouST23°09′ N 116°38′ E2020.1228
Total 233
Table 2. Genetic diversity analysis of eight N. yoldii populations based on COI gene.
Table 2. Genetic diversity analysis of eight N. yoldii populations based on COI gene.
PopulationShHdKPiPiJC
SS1090.52820.95970.00190.0020
LH540.22920.41670.00080.0009
XS980.54941.25750.00260.0026
TZ860.60921.58160.00320.0032
FD870.52310.96310.00200.0020
XP880.72871.80460.00370.0037
XM13110.75361.44200.00290.0029
ST13120.74871.44180.00290.0029
Total34340.58381.23340.0025
S, mutation sites; h, haplotype numbers; Hd, haplotype diversity; K, average number of pairwise divergences; Pi, nucleotide diversity; PiJC, nucleotide diversity with JC.
Table 3. AMOVA analysis of eight N. yoldii populations based on COI gene.
Table 3. AMOVA analysis of eight N. yoldii populations based on COI gene.
Source of Variationd.f.Sum of SquaresVariance ComponentsPercentage of Variation
Among populations78.5930.02127 Va3.38
Within populations225136.9610.60872 Vb96.62
Total232145.5540.62999
Table 4. The neutral test of eight N. yoldii populations based on COI gene.
Table 4. The neutral test of eight N. yoldii populations based on COI gene.
StatisticsSSLHXSTZFDXPXMSTMeans.d.
Tajima’s D−1.92−1.76−1.39−0.66−1.70−0.32−2.03−1.90−1.460.63
Tajima’s D p-value0.010.010.070.280.030.420.010.010.100.16
FS−5.40−1.55−3.00−0.30−3.14−1.65−7.16−8.07−3.782.80
FS p-value0.000.060.030.460.010.190.000.000.090.16
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

Jiang, S.; Li, Z.; Li, J.; Xu, K.; Ye, Y. Analysis of Genetic Diversity and Structure of Eight Populations of Nerita yoldii along the Coast of China Based on Mitochondrial COI Gene. Animals 2024, 14, 718. https://doi.org/10.3390/ani14050718

AMA Style

Jiang S, Li Z, Li J, Xu K, Ye Y. Analysis of Genetic Diversity and Structure of Eight Populations of Nerita yoldii along the Coast of China Based on Mitochondrial COI Gene. Animals. 2024; 14(5):718. https://doi.org/10.3390/ani14050718

Chicago/Turabian Style

Jiang, Senping, Zhenhua Li, Jiji Li, Kaida Xu, and Yingying Ye. 2024. "Analysis of Genetic Diversity and Structure of Eight Populations of Nerita yoldii along the Coast of China Based on Mitochondrial COI Gene" Animals 14, no. 5: 718. https://doi.org/10.3390/ani14050718

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop