Skip to main content
SpringerLink
Log in

Population Genetic Structure of Liza affinis (Eastern Keelback Mullet), Reveals High Gene Flow Inferred from Microsatellite Analysis

  • Article
  • Published:
Ocean Science Journal Aims and scope Submit manuscript

Abstract

The population genetic studies of marine fishes usually show complex patterns of genetic differentiation which were influenced by both historical process and contemporary gene flow. Genetic structure of eight different populations for eastern keelback mullet, Liza affinis, collected from the coast along eastern and southern China, was examined using six microsatellite loci. We found strong genetic similarities among most of the samples except the Dongguan population and most microsatellite variation was found within populations. All loci were characterized by high genetic variability with expected heterozygosities ranging from 0.871 to 0.928. The Bayesian cluster analysis of the microsatellite data detected four genetic groups with no relation to geographic areas. The bottleneck results also showed no significant values. Based on these data we postulated that complex marine currents and larval dispersal shaped the genetic structured of studied populations. The present study illustrated the importance of understanding the biological significance of genetic differentiation when using molecular data in identifying units for management and protection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, 447 p

    Google Scholar 

  • Banks MA, Blouin MS, Baldwin BA, Rashbrook VK, Fitzgerald HA, Blankenship SM, Hedgecock D (1999) Isolation and inheritance of novel microsatellites in chinook salmon (Oncorhynchus tschawytscha). J Hered 90(2):281–288

    Article  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2002) GENETIX 4.05, logiciel sous Windows TM pour la Génétique des Populations. Université de Montpellier II, Montpellier (in French)

    Google Scholar 

  • Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74(1):21–45

    Article  Google Scholar 

  • Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. J Hered 93:153–154

    Article  Google Scholar 

  • Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32:314–331

    Google Scholar 

  • Carlsson J, McDowell JR, Diaz-Jaimes P, Carlsson JE, Bole SB, Gold JR, Graves JE (2004) Microsatellite and mitochondrial DNA analyses of Atlantic bluefin tuna (Thunnus thynnus thynnus) population structure in the Mediterranean Sea. Mol Ecol 13:3345–3356

    Article  Google Scholar 

  • Cheng J, Yanagimoto T, Song N, Gao TX (2015) Population genetic structure of chub mackerel Scomber japonicus in the Northwestern Pacific inferred from microsatellite analysis. Mol Biol Rep 42:373–382

    Article  Google Scholar 

  • Diáz-Ferguson E, Haney RA, Wares JP, Silliman BR (2010) Population genetics of a trochid gastropod broadens picture of Caribbean Sea connectivity. PLoS One 5:e12675. doi:https://doi.org/10.1371/journal.pone.0012675

    Article  Google Scholar 

  • Durand JD, Blel H, Shen KN, Koutrakis ET, Guinand B (2013) Population genetic structure of Mugil cephalus in the Mediterranean and Black Seas: a single mitochondrial clade and many nuclear barriers. Mar Ecol-Prog Ser 474:243–261

    Article  Google Scholar 

  • Earl DA (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Falconer DS, Mackayt FC (1996) Introduction to quantitative genetics. The Ronald Press Company, New York, 480 p

    Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164(4):1567–1587

    Google Scholar 

  • Ferreira ME, Grattapaglia D (1998) Introdução ao uso de marcadores moleculares em análise genética. Embrapa, Brasília, 220 p

    Google Scholar 

  • Gao TX, Han ZQ, Zhang XM, Luo J, Yanagimoto T, Zhang H (2016) Population genetic differentiation of the black rockfish Sebastes schlegelii revealed by microsatellites. Biochem Syst Ecol 68:170–177

    Article  Google Scholar 

  • Gong XL, Zhu WJ, Bao BL (2016) Complete mitochondrial DNA sequence of the Eastern keelback mullet Liza affinis. Mitochondr DNA 27:2178–2179

    Google Scholar 

  • Goudet J (2001) FSTAT V.2.9.3, a program to estimate and test gene diversities and fixation indices (Updated from Goudet 1995). University of Lausanne. http://www.unil.ch/izea/softwares/fstat.html Accessed 9 Sep 2017

    Google Scholar 

  • Guan BX, Fang GH (2006) Winter counter-wind currents off the southeastern China coast: a review. J Oceanogr 62:1–24

    Article  Google Scholar 

  • Gyllensten U (1985) The genetic structure of fish: differences in the intraspecific distribution of biochemical genetic variation between marine, anadromous and freshwater species. J Fish Biol 26:691–699

    Article  Google Scholar 

  • Hu J, Kawamura H, Hong H, Qi Y (2000) A review on the currents in the South China Sea: seasonal circulation, South China Sea Warm Current and Kuroshio intrusion. J Oceanogr 56(6): 607–624

    Article  Google Scholar 

  • Hwang J, Wong C (2005) The China Coastal Current as a driving force for transporting Calanus sinicus (Copepoda: Calanoida) from its population centers to waters off Taiwan and Hong Kong during the winter northeast monsoon period. J Plankton Res 27(2):205–210

    Article  Google Scholar 

  • Lee CL, Joo DS (1994) Synopsis of family Mugilidae (Perciformes) from Korea. Bull Korean Fish Soc 27:814–824

    Google Scholar 

  • Ikeda T, Mito S (1988) The identification of fish eggs and emergent larvae. In: Okiyama M (ed) An atlas of the early stage fishes in Japan. Tokai University Press, Tokyo, pp 999–1083 (in Japanese)

    Google Scholar 

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13. doi:https://doi.org/10.1186/1471-2156-6-13

    Article  Google Scholar 

  • Joh YG, Lee KH, Cho YJ (1988) Lipid composition of roe, muscle and viscus of Liza carinata, a species of the Mugilidae family. J Food Sci Tech Mys 20:674–682

    Google Scholar 

  • Jones AG, Stockwell CA, Walker D, Avise JC (1998) The molecular basis of a microsatellite null allele from the white sands pupfish. J Hered 89:339–342

    Article  Google Scholar 

  • Kim MJ, An HS, Choi KH (2010a) Genetic characteristics of Pacific cod populations in Korea based on microsatellite markers. Fisheries Sci 76:595–603

    Article  Google Scholar 

  • Kim WJ, Kim KK, Han HS, Nam BH, Kim YO, Kong HJ, Noh JK, Yoon, M (2010b) Population structure of the olive flounder (Paralichthys olivaceus) in Korea inferred from microsatellite marker analysis. J Fish Biol 76:1958–1971

    Article  Google Scholar 

  • Kinoshita I (1988) Liza carinata carinata in Mugilidae. In: Okiyama M (ed) An atlas of the early stage fishes in Japan. Tokai University Press, Tokyo, pp 390–391 (in Japanese)

    Google Scholar 

  • Kvie KS, Hogner S, Aarvik L, Lifjeld JT, Johnsen A (2013) Deep sympatric mtDNA divergence in the autumnal moth (Epirrita autumnata). Ecol Evol 3(1):126–144

    Article  Google Scholar 

  • Largier JL (2003) Considerations in estimating larval dispersal distances from oceanographic data. Ecol Appl 13(1):S71–S89

    Article  Google Scholar 

  • Liao XJ, Chang H, Sun W (2006) Study of genetic diversity in six sheep/goat population with microsatellite markers. Acta Ecol Ani Dom 27(2):13–18 (in Chinese)

    Google Scholar 

  • Li WQ, Zheng WY, Cai AG, Chen WQ (1993) The study on the diet ingestion, absorption and utilization of Liza carinatus. Mar Sci 2:43–47 (in Chinese)

    Google Scholar 

  • Liu JY, Brown CL, Yang TB (2009) Population genetic structure and historical demography of grey mullet, Mugil cephalus, along the coast of China, inferred by analysis of the mitochondrial control region. Biochem Syst Ecol 37:556–566

    Article  Google Scholar 

  • Liu L, Gao TX, Han ZQ, Li CH, Sun DR, Song N (2016a) Latin name correction of Liza affinis from China. J Fish Sci China 23(5):1108–1116 (in Chinese)

    Google Scholar 

  • Liu L, Gao TX, Han ZQ, Li CH, Sun DR, Song N (2016b) Development and characterization of microsatellite markers of the eastern keelback mullet (Liza affinis). Genet Mol Res 15(2):1–4

    Google Scholar 

  • Liu L, Panhwar SK, Gao TX, Han ZQ, Li CH, Sun DR, Song N (2017) New genetic evidence from three keel-backed Liza species based on DNA barcoding confirms morphology-based Identification. Pak J Zool 49(5):1901–1907

    Article  Google Scholar 

  • Liu L, Liu LQ, Gao TX, Song N (2018) Phylogeographic pattern of Liza affinis populations in Chinese coastal waters: estimation of larval dispersal potential. Mitochondr DNA 29:1253–1260. doi:https://doi.org/10.1080/24701394.2018.1444038

    Article  Google Scholar 

  • Mai AC, Mino CI, Marins LF, Monteiro-Neto C, Miranda L, Schwingel PR, Lemos VM, Gonzalez-Castro M, Castello JP, Vieira JP (2014) Microsatellite variation and genetic structuring in Mugil liza (Teleostei: Mugilidae) populations from Argentina and Brazil. Estuar Coast Shelf S 149:80–86

    Article  Google Scholar 

  • Minegishi Y, Aoyama J, Tsukamoto K (2008) Multiple population structure of the giant mottled eel, Anguilla marmorata. Mol Ecol 17:3109–3122

    Article  Google Scholar 

  • Mito S (1966) Fish eggs and larvae. In: Okiyama M (ed) An atlas of the early stage fishes in Japan. Tokai University Press, Tokyo, pp 44–45 (in Japanese)

    Google Scholar 

  • Moritz C, Dowling TE, Brown WM (1987) Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annu Rev Ecol Syst 18:269–292

    Article  Google Scholar 

  • Nakamura S (1936) Larvae and young of fishes found in the vicinity of Kominato —XV. J Imp Fish Inst 7:135–144 (in Japanese)

    Google Scholar 

  • Nash CE, Shehadeh ZH (1980) Review of breeding and propagation techniques for grey mullet, Mugil cephalus L. ICLARM Stu Rev 3:11–77

    Google Scholar 

  • Nielsen EE, Hansen MM, Schmidt C, Meldrup D, Grønkjaer P (2001) Population of origin of Atlantic cod. Nature 413:272

    Article  Google Scholar 

  • Novembre J, Johnson T, Bryc K, Kutalik Z, Boyko AR, Auton A, Indap A, King KS, Bergmann S, Nelson MR, Stephens M, Bustamante CD (2008) Genes mirror geography within Europe. Nature 456:98–101

    Article  Google Scholar 

  • Oliver L (2002) Populations 1.2.28. http://www.cnrs-gif.fr/pge/bioinfo/populations Accessed 9 Sep 2017

    Google Scholar 

  • Olivier L, Wolf YI, Koonin EV, Aravind L (2012) The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res 12:1048–1059

    Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annul Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Park SDE (2001) Trypanotolerance in West African cattle and the population genetic effects of selection. Ph.D. Thesis, University of Dublin

    Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90(4):502–503

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genet 155(2):945–959

    Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP Version 1.2: population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  • Rocha-Olivares A, Garber NM, Stuck KC (2000) High genetic diversity, large inter-oceanic divergence and historical demography of the striped mullet. J Fish Biol 57:1134–1149

    Article  Google Scholar 

  • Rocha-Olivares A, Garber NM, Garber AF, Stuck KC (2017) Structure of the mitochondrial control region and flanking tRNA genes of Mugil cephalus. Hidrobiologica 15:139–149

    Google Scholar 

  • Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Sambrook J, Russell DW (2001) Gel electrophoresis of DNA and pulsed-field agarose gel electrophoresis. In: Green MR, Sambrook J (eds) Molecular cloning: a laboratory manual. Cold Spring Harbor laboratory press, New York, pp 5.4–5.86

    Google Scholar 

  • Selkoe KA, Aloia CCD, Crandall ED, Lacchei M, Liggins L, Puritz JB, Heyden SVD, Toonen RJ (2016) A decade of seascape genetics: contributions to basic and applied marine connectivity. Mar Ecol-Prog Ser 554:1–19

    Article  Google Scholar 

  • Stoneking M, Hedgecock D, Higuchi RG, Vigilant L, Erlich HA (1991) Population variation of human mtDNA control region sequences detected by enzymatic amplification and sequence-specific oligonucleotide probes. Am J Hum Genet 48(2):370–382

    Google Scholar 

  • Su JL (2004) Overview of the South China Sea circulation and its influence on the coastal physical oceanography outside the Pearl River Estuary. Cont Shelf Res 24:1745–1760

    Article  Google Scholar 

  • Toews DPL, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21:3907–3930

    Article  Google Scholar 

  • Tsang LM, Chan BKK, Ma KY, Chu KH (2008) Genetic differentiation, hybridization and adaptive divergence in two subspecies of the acorn barnacle Tetraclita japonica in the northwestern Pacific. Mol Ecol 17:4151–4163

    Article  Google Scholar 

  • Van OC, Hutchinson WF, Wills DPM, Shipley P (2004) MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:439–450

    Article  Google Scholar 

  • Ward RD (2006) The importance of identifying spatial population structure in restocking and stock enhancement programmes. Fish Res 80:9–18

    Article  Google Scholar 

  • Ward RD, Woodwark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater and anadromous fishes. J Fish Biol 44:213–232

    Article  Google Scholar 

  • Webb WC, Marzluff JM, Omland KE (2011) Random interbreeding between cryptic lineages of the Common Raven: evidence for speciation in reverse. Mol Ecol 20:2390–2402

    Article  Google Scholar 

  • Whitfield AK, Panfili J, Durand JD (2012) A global review of the cosmopolitan flathead mullet Mugil cephalus Linnaeus 1758 (Teleostei: Mugilidae), with emphasis on the biology, genetics, ecology and fisheries aspects of this apparent species complex. Rev Fish Biol Fisher 22:641–681

    Article  Google Scholar 

  • Yang SY, Qiu SY (1989) A preliminary study on growth and feeding habits of Mullet (Liza carinata) underyearlings in Luoyuan Bay. J Xiamen Univ 28:110–119 (in Chinese)

    Google Scholar 

  • Yoshimatsu T, Matsui S, Kitajima C (1993) Early development of laboratory-reared keelback mullet. Nippon Suisan Gakk 59(5): 765–776

    Article  Google Scholar 

  • Yuan M, Tang Y, Xu SN, Chen ZZ, Yang YT, Jiang YE (2017) Community structure of fishery resources from the Nansha Waters of Pearl River Estuary in autumn. South China Fisher Sci 13:18–25 (in Chinese)

    Google Scholar 

  • Zhang DX, Hewitt GM (2003) Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Mol Ecol 12:563–584

    Article  Google Scholar 

  • Zhang R, Lu S, Zhao CY, Chen L, Zang Z, Zhang X (1985) Fish eggs and larvae in the offshore waters of China. Shanghai Sci Tech Press, Shanghai, 206 p

    Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (41506158, 41776171) and the Special Fund for Agro-scientific Research in the Public Interest (201303048). We thank Dr. Yuan Li, Dr. Liangmin Huang, Mr. Binbin Shan, Mr. Long Yan for collecting the samples. We also thank Dr. Jiaguang Xiao and Mr. Wei Zhou for their help in data processing.

Author information

Authors and Affiliations

  1. The Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, 276000, China

    Lu Liu & Na Song

  2. National Engineering Research Center for Marine Aquaculture, Zhejiang Ocean University, Zhoushan, 316021, China

    Xiumei Zhang & Tianxiang Gao

  3. South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, 510300, China

    Dianrong Sun

  4. Key Laboratory for Technology Research on Sustainable Utilization of Marine Fishery Resources, Zhoushan, 316021, China

    Tianxiang Gao

Authors
  1. Lu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiumei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dianrong Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tianxiang Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Na Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Na Song.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, L., Zhang, X., Sun, D. et al. Population Genetic Structure of Liza affinis (Eastern Keelback Mullet), Reveals High Gene Flow Inferred from Microsatellite Analysis. Ocean Sci. J. 54, 245–256 (2019). https://doi.org/10.1007/s12601-019-0013-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12601-019-0013-y

Keywords

Search

Navigation