Abstract
Genetic diversity and population structure are fundamental to studying population dynamics and understanding demographic history, playing a key role in marine organism conservation. To study the genetic diversity and population structure of whitespotted conger Conger myriaster, an important commercial marine species, broadly distributed in Asia, a total of 197 individuals were collected from six locations along the East China Coast. Around 655 bp sequence of mitochondrial control region was used to assess the genetic diversity, population differentiation, and demographic history of C. myriaster populations. A high level of haplotype diversity was detected. No significant population structure was observed by using analysis of molecular variance (AMOVA), consistent with the results of discriminant analysis of principal components (DAPC) and Mantel tests. Bayesian phylogenetic tree revealed three distinct lineages, which diverged during the Pleistocene. Mismatch and Bayesian skyline analyses supported that all geographical populations as well as three evolutionary lineages had experienced demographic expansions. This genetic assessment would give an important contribution to revealing the interaction between phylogeographic history and demographic history and future utilization and conservation of this species.
Similar content being viewed by others
References
Avise JC (2009) Phylogeography: retrospect and prospect. J Biogeogr 36:3–15. https://doi.org/10.1111/j.1365-2699.2008.02032.x
Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522. https://doi.org/10.1146/annurev.es.18.110187.002421
Bernatchez L (1997) Mitochondrial DNA analysis confirms the existence of two glacial races of rainbow smelt Osmerus mordax and their reproductive isolation in the St Lawrence River estuary (Quebec, Canada). Mol Ecol 6:73–83. https://doi.org/10.1046/j.1365-294X.1997.00156.x
Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Brito PH, Edwards SV (2009) Multilocus phylogeography and phylogenetics using sequence-based markers. Genetica 135:439–455. https://doi.org/10.1007/s10709-008-9293-3
Callaerts P, Zhang Y, Pham NK, Zhang H, Lin J, Lin Q (2014) Genetic variations in two seahorse species (Hippocampus mohnikei and Hippocampus trimaculatus): evidence for middle Pleistocene population expansion. PLoS ONE 9:e105494. https://doi.org/10.1371/journal.pone.0105494
Canales-Aguirre CB, Ferrada-Fuentes S, Galleguillos R, Oyarzun FX, Buratti CC, Hernández CE (2018) High genetic diversity and low-population differentiation in the Patagonian sprat (Sprattus fuegensis) based on mitochondrial DNA. Mitochondrial DNA. Part A, DNA Mapping, Sequencing, and Analysis 29: 1148–1155. https://doi.org/10.1080/24701394.2018.1424841
Cheng Q, Zheng B (1987) Systematic synopsis of Chinese fishes. Science Press, Beijing
Cheng J, Han Z, Song N, Gao T, Yanagimoto T, Strüssmann CA (2018) Effects of Pleistocene glaciation on the phylogeographic and demographic histories of chub mackerel Scomber japonicus in the North-Western Pacific. Mar Freshw Res 69:514. https://doi.org/10.1071/MF17099
Clement M, Posada D, Crandall KA (2001) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and high-performance computing. Nat Methods 9:772–772. https://doi.org/10.1038/nmeth.2109
Delrieu-Trottin E, Neglia V, Verducci M, Planes S (2018) Origin, genetic diversity, and population history of a marine population (Chanidae: Chanos chanos) in an enclosed lagoon in French Polynesia. Pac Sci 72:223–231. https://doi.org/10.2984/72.2.4
Domingues RR, Hilsdorf AWS, Shivji MM, Hazin FVH, Gadig OBF (2018) Effects of the Pleistocene on the mitochondrial population genetic structure and demographic history of the silky shark (Carcharhinus falciformis) in the Western Atlantic Ocean. Rev Fish Biol Fish 28:213–227. https://doi.org/10.1007/s11160-017-9504-z
Donaldson KA, Wilson RR (1999) Amphi-panamic geminates of snook (Percoidei: Centropomidae) provide a calibration of the divergence rate in the mitochondrial DNA control region of fishes. Mol Phylogenet Evol 13:208–213. https://doi.org/10.1006/mpev.1999.0625
Excoffier L (2003) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864. https://doi.org/10.1046/j.1365-294X.2003.02004.x
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 Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Féral JP (2002) How useful are the genetic markers in attempts to understand and manage marine biodiversity? J Exp Mar Biol Ecol 268:121–145. https://doi.org/10.1016/S0022-0981(01)00382-3
Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496. https://doi.org/10.1016/j.tree.2012.05.012
Gagne TO, Reygondeau G, Jenkins CN, Sexton JO, Bograd SJ, Hazen EL, Van Houtan KS (2020) Towards a global understanding of the drivers of marine and terrestrial biodiversity. PLoS ONE 15:e0228065. https://doi.org/10.1371/journal.pone.0228065
Gong XL, Ren SJ, Cui ZK, Yue LJ (2014) Genetic evidence for panmixia of Japanese eel (Anguilla japonica) populations in China. Genet Mol Res 13:768–781. https://doi.org/10.4238/2014.January.31.3
Han ZQ, Gao TX, Yanagimoto T, Sakurai Y (2008) Genetic population structure of Nibea albiflora in Yellow Sea and East China Sea. Fish Sci 74:544–552. https://doi.org/10.1111/j.1444-2906.2008.01557.x
Han Z, Yanagimoto T, Zhang Y, Gao T (2012) Phylogeography study of Ammodytes personatus in Northwestern Pacific: Pleistocene isolation, temperature and current conducted secondary contact. PLoS One 7:e37425. https://doi.org/10.1371/journal.pone.0037425
He L, Zhang A, Weese D, Zhu C, Jiang C, Qiao Z (2010) Late Pleistocene population expansion of Scylla paramamosain along the coast of China: a population dynamic response to the last interglacial sea level highstand. J Exp Mar Biol Ecol 385:20–28. https://doi.org/10.1016/j.jembe.2010.01.019
He L, Mukai T, Chu KH, Ma Q, Zhang J (2015) Biogeographical role of the Kuroshio current in the amphibious mudskipper Periophthalmus modestus indicated by mitochondrial DNA data. Sci Rep 5:15645. https://doi.org/10.1038/srep15645
Inoue K, Monroe EM, Elderkin CL, Berg DJ (2014) Phylogeographic and population genetic analyses reveal Pleistocene isolation followed by high gene flow in a wide ranging, but endangered, freshwater mussel. Heredity 112:282–290. https://doi.org/10.1038/hdy.2013.104
Ishikawa S, Kimura Y, Tokai T, Tsukamoto K, Nishida M (2001) Genetic variation in the mitochondrial and nuclear DNA of the Japanese conger Conger myriaster. Fish Sci 67:1081–1087. https://doi.org/10.1046/j.1444-2906.2001.00364.x
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Ketchum RN, Dieng MM, Vaughan GO, Burt JA, Idaghdour Y (2016) Levels of genetic diversity and taxonomic status of Epinephelus species in United Arab Emirates fish markets. Mar Pollut Bull 105:540–545. https://doi.org/10.1016/j.marpolbul.2015.11.042
Lambeck K, Esat TM, Potter EK (2002) Links between climate and sea levels for the past three million years. Nature 419:199. https://doi.org/10.1038/nature01089
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404
Li H, Lin H, Li J, Ding S (2014) Phylogeography of the Chinese beard eel, Cirrhimuraena chinensis Kaup, inferred from mitochondrial DNA: a range expansion after the last glacial maximum. Int J Mol Sci 15:13564–13577. https://doi.org/10.3390/ijms150813564
Liang Y, He D, Jia Y, Sun H, Chen Y (2017) Phylogeographic studies of schizothoracine fishes on the central Qinghai-Tibet Plateau reveal the highest known glacial microrefugia. Sci Rep 7:10983. https://doi.org/10.1038/s41598-017-11198-w
Lie HJ, Cho CH (2016) Seasonal circulation patterns of the Yellow and East China Seas derived from satellite-tracked drifter trajectories and hydrographic observations. Prog Oceanogr 146:121–141. https://doi.org/10.1016/j.pocean.2016.06.004
Lin HC, Chen JP, Chan BKK, Shao KT (2014) The interplay of sediment characteristics, depth, water temperature, and ocean currents shaping the biogeography of lancelets (Subphylum Cephalochordata) in the NW Pacific waters. Mar Ecol 36:780–793. https://doi.org/10.1111/maec.12183
Liu JX, Gao TX, Yokogawa K, Zhang YP (2006) 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 39:799–811. https://doi.org/10.1016/j.ympev.2006.01.009
Liu JX, Gao TX, Wu SF, Zhang YP (2007) Pleistocene isolation in the northwestern Pacific marginal seas and limited dispersal in a marine fish, Chelon haematocheilus (Temminck & Schlegel, 1845). Mol Ecol 16:275–288. https://doi.org/10.1111/j.1365-294X.2006.03140.x
Liu BJ, Zhang BD, Xue DX, Gao TX, Liu JX (2016) Population structure and adaptive divergence in a high gene flow marine fish: the small yellow croaker (Larimichthys polyactis). PLoS ONE 11:e0154020. https://doi.org/10.1371/journal.pone.0154020
Ma T, Miller MJ, Aoyama J, Tsukamoto K (2007) Genetic identification of Conger myriaster leptocephali in East China Sea. Fish Sci 73:989–994. https://doi.org/10.1111/j.1444-2906.2007.01427.x
Ma QY, Mu XX, Ren YP, Sun YY (2018) The growth, mortality and yield per recruitment of white-spotted conger (Conger myriaster) in the Yellow Sea and the East China Sea. J Fish China 42:881–888. https://doi.org/10.11964/jfc.20171111040
Madduppa HH, Timm J, Kochzius M (2018) Reduced genetic diversity in the clown anemonefish Amphiprion ocellaris in exploited reefs of Spermonde Archipelago, Indonesia. Front Mar Sci 5:80. https://doi.org/10.3389/fmars.2018.00080
Makhrov AA, Lajus DL (2018) Postglacial colonization of the north European seas by Pacific fishes and lamprey. Contemp Probl Ecol 11:247–258. https://doi.org/10.1134/S1995425518030071
Manel S, Guerin PE, Mouillot D, Blanchet S, Velez L, Albouy C, Pellissier L (2020) Global determinants of freshwater and marine fish genetic diversity. Nat Commun 11:1–9. https://doi.org/10.1038/s41467-020-14409-7
Melis R, Vacca L, Cuccu D, Mereu M, Cau A, Follesa MC, Cannas R (2018) Genetic population structure and phylogeny of the common octopus Octopus vulgaris Cuvier, 1797 in the western Mediterranean Sea through nuclear and mitochondrial markers. Hydrobiologia 807:277–296. https://doi.org/10.1007/s10750-017-3399-5
Miller MJ (2009) Ecology of anguilliform leptocephali: remarkable transparent fish larvae of the ocean surface layer. Aqua-BioSci Monogr 2:1–94. https://doi.org/10.5047/absm.2009.00204.0001
Minagawa G, Miller MJ, Kimura Y, Watanabe S, Shinoda A, Aoyama J, Tsukamoto K (2007) Seasonal differences in catches of leptocephali in the East China Sea and Suruga Bay, Japan. Estuar Coast Shelf Sci 71:730–740. https://doi.org/10.1016/j.ecss.2006.06.018
Miralles L, Lee LS, Borrell Y, Garcia-Vazquez E (2016) Population genetic structure of the European conger (Conger conger) in north East Atlantic and West Mediterranean Sea. Fish Res 174:245–249. https://doi.org/10.1016/j.fishres.2015.10.013
Mukai T, Nakamura S, Nishida M (2009) Genetic population structure of a reef goby, Bathygobius cocosensis, in the northwestern Pacific. Ichthyol Res 56:380. https://doi.org/10.1007/s10228-009-0111-4
Nei M (1987) Molecular evolutionary genetics, vol 237. Columbia University Press, p 599
Neiva J, Paulino C, Nielsen MM, Krause-Jensen D, Saunders GW, Assis J, Bárbara I, Tamigneaux É, Gouveia L, Aires T, Marbà N, Bruhn A, Pearson GA, Serrão EA (2018) Glacial vicariance drives phylogeographic diversification in the amphi-boreal kelp Saccharina latissima. Sci Rep 8:1112. https://doi.org/10.1038/s41598-018-19620-7
Ni G, Li Q, Kong L, Zheng X (2012) Phylogeography of bivalve Cyclina sinensis: testing the historical glaciations and Changjiang River outflow hypotheses in northwestern Pacific. PLoS One 7:e49487. https://doi.org/10.1371/journal.pone.0049487
Ni G, Li Q, Kong LF, Yu H (2014) Comparative phylogeography in marginal seas of the northwestern Pacific. Mol Ecol 23:534–548. https://doi.org/10.1111/mec.12620
Okamura A, Utoh T, Zhang H, Yamada Y, Horie N, Mikawa N, Tanaka S, Motonobu T, Oka HP (2000) Seasonal changes in maturity in the conger eel Conger myriaster at the Pacific coast of Atsumi Peninsula, central Japan. Nippon Suisan Gakkaishi 66:412–416. https://doi.org/10.2331/suisan.66.412
Östman Ö, Olsson J, Dannewitz J, Palm S, Florin AB (2016) Inferring spatial structure from population genetics and spatial synchrony in demography of Baltic Sea fishes: implications for management. Fish Fish 18:324–339. https://doi.org/10.1111/faf.12182
Otwoma LM, Reuter H, Timm J, Meyer A (2018) Genetic connectivity in a herbivorous coral reef fish (Acanthurus leucosternon Bennet, 1833) in the eastern African region. Hydrobiologia 806:237–250. https://doi.org/10.1007/s10750-017-3363-4
Pfeiler E (1999) Developmental physiology of elopomorph leptocephali. Comp Biochem Physiol A Mol Integr Physiol 123:113–128. https://doi.org/10.1016/s1095-6433(99)00028-8
Pillans B, Chappell J, Naish TR (1998) A review of the Milankovitch climatic beat: template for Plio-Pleistocene sea-level changes and sequence stratigraphy. Sediment Geol 122:5–21. https://doi.org/10.1016/S0037-0738(98)00095-5
Provan J, Bennett K (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23:564–571. https://doi.org/10.1016/j.tree.2008.06.010
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67(5):901–904. https://doi.org/10.1093/sysbio/syy032
Ramírez-Soriano A, Ramos-Onsins SE, Rozas J, Calafell F, Navarro A (2008) Statistical power analysis of neutrality tests under demographic expansions, contractions and bottlenecks with recombination. Genetics 179:555–567. https://doi.org/10.1534/genetics.107.083006
Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100. https://doi.org/10.1093/oxfordjournals.molbev.a004034
Rodrigues R, Schneider H, Santos S, Vallinoto M, Sain-Paul U, Sampaio I (2008) Low levels of genetic diversity depicted from mitochondrial DNA sequences in a heavily exploited marine fish (Cynoscion acoupa, Sciaenidae) from the northern coast of Brazil. Genet Mol Biol 31:487–492. https://doi.org/10.1590/S1415-47572008000300015
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089
Shui BN, Han ZQ, Gao TX, Miao ZQ, Yanagimoto T (2009) Mitochondrial DNA variation in the East China Sea and Yellow Sea populations of Japanese Spanish mackerel Scomberomorus niphonius. Fish Sci 75:593–600. https://doi.org/10.1007/s12562-009-0083-3
Tamaki K, Honza E (1991) Global tectonics and formation of marginal basins: role of the Western Pacific. Trans World Seismol 14:224–230. https://doi.org/10.18814/epiiugs/1991/v14i3/005
Truelove NK, Box SJ, Aiken KA, Blythe-Mallett A, Boman EM, Booker CJ, Byfield TT, Cox CE, Davis M, Delgado GA, Glazer BA, Griffiths S, Kitson-Walters K, Kough AS, Enríquez RP, Preziosi RF, Roy ME, Segura-Garcia I, Webber MK, Stoner AW (2017) Isolation by oceanic distance and spatial genetic structure in an overharvested international fishery. Divers Distrib 23:1292–1300. https://doi.org/10.1111/ddi.12626
Utoh T, Horie N, Okamura A, Mikawa N, Yamada Y, Tanaka S, Oka HP, Tsukamoto K (2013) Water temperature manipulation can induce oocyte maturation and ovulation in the common Japanese conger, Conger myriaster. Aquaculture 392-395:120–127. https://doi.org/10.1016/j.aquaculture.2013.02.007
Wang P (1999) Response of Western Pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features. Mar Geol 156:5–39. https://doi.org/10.1016/S0025-3227(98)00172-8
Wang Q, Zhang J, Matsumoto H, Kim JK, Li C (2016) Population structure of elongate ilisha Ilisha elongata along the Northwestern Pacific Coast revealed by mitochondrial control region sequences. Fish Sci 82:771–785. https://doi.org/10.1007/s12562-016-1018-4
Wang X, Kong L, Chen J, Matsukuma A, Li Q (2017) Phylogeography of bivalve Meretrix petechialis in the Northwestern Pacific indicated by mitochondrial and nuclear DNA data. PLoS ONE 12:e0183221. https://doi.org/10.1371/journal.pone.0183221
Watanabe S, Hagihara S, Miller MJ, Machida M, Komatsu K, Nishida S, Tsukamoto K (2016) Collection of spawning-condition eels of Ariosoma meeki in the Kuroshio current in the East China Sea. J Mar Biol Assoc U K 96:1701–1707. https://doi.org/10.1017/S002531541500209X
Wee AKS, Takayama K, Asakawa T, Thompson B, Onrizal SS, Tung NX, Nazre M, Soe KK, Tan HTW, Watano Y, Baba S, Kajita T, Webb EL (2014) Oceanic currents, not land masses, maintain the genetic structure of the mangrove Rhizophora mucronata Lam. (Rhizophoraceae) in Southeast Asia. J Biogeogr 41:954–964. https://doi.org/10.1111/jbi.12263
Xiao Y, Zhang Y, Gao T, Yanagimoto T, Yabe M, Sakurai Y (2009) Genetic diversity in the mtDNA control region and population structure in the small yellow croaker Larimichthys polyactis. Environ Biol Fish 85:303–314. https://doi.org/10.1007/s10641-009-9497-0
Yagi Y, Kodono N, Kinoshita I, Fujita S (2010) Late-stage metamorphosing Conger myriaster leptocephali collected in a river estuary of Ariake Bay, Japan. Ichthyol Res 57:310–313. https://doi.org/10.1007/s10228-010-0154-6
Zhang D, Ding G, Ge B, Zhang H, Tang B, Yang G (2014) Comparative phylogeography of two marine species of crustacean: recent divergence and expansion due to environmental changes. Gene 550:141–147. https://doi.org/10.1016/j.gene.2014.08.006
Acknowledgments
We are grateful to Prof. Mengxia Liu and Dr. Wei Liu, in the Marine Biology Institute of Shandong Province, for sample collection in the field. We also thank the anonymous referees for their comments and suggestions which greatly helped to improve the manuscript.
Funding
This study was funded by the Major Agricultural Application Technology and Innovation Project of Shandong Province (2017–2020), Special Program for Basic Research of the Ministry of Science and Technology of China (No. 2014FY110500), and the National Infrastructure of Fishery Germplasm Resource (No. 2017DKA30470).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.
Sampling and field studies
All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable.
Data availability
All mitochondrial control region haplotypes were registered in GenBank under accession numbers MK030178-MK030340. The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
Authors’ contribution
Congcong Zou and Lijuan Wang designed and performed the experiments, analyzed the data, and wrote the manuscript. Feng You conceived the experiments and revised the manuscript. Lingming Kong participated in the data analysis. Yingjun Wang, Jianhe Xu, Aihuan Song, and Hongjun Liu collected and prepared the fish samples. Zhihao Wu carried out the sample identification. All authors read and approved the manuscript.
Additional information
Communicated by R. Thiel
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Congcong Zou and Lijuan Wang contribute the same to this paper
Electronic supplementary material
ESM 1
(PDF 242 kb)
Rights and permissions
About this article
Cite this article
Zou, C., Wang, L., Kong, L. et al. High levels of genetic diversity and connectivity of whitespotted conger Conger myriaster in the East China Coast. Mar. Biodivers. 50, 47 (2020). https://doi.org/10.1007/s12526-020-01071-x
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12526-020-01071-x