Volume 41 Issue 1
Jan.  2020
Turn off MathJax
Article Contents
Xing-Han Chen, Sen Yang, Wei Yang, Yuan-Yuan Si, Rui-Wen Xu, Bin Fan, Le Wang, Zi-Ning Meng. First genetic assessment of brackish water polychaete Tylorrhynchus heterochaetus: mitochondrial COI sequences reveal strong genetic differentiation and population expansion in samples collected from southeast China and north Vietnam. Zoological Research, 2020, 41(1): 61-69. doi: 10.24272/j.issn.2095-8137.2020.006
Citation: Xing-Han Chen, Sen Yang, Wei Yang, Yuan-Yuan Si, Rui-Wen Xu, Bin Fan, Le Wang, Zi-Ning Meng. First genetic assessment of brackish water polychaete Tylorrhynchus heterochaetus: mitochondrial COI sequences reveal strong genetic differentiation and population expansion in samples collected from southeast China and north Vietnam. Zoological Research, 2020, 41(1): 61-69. doi: 10.24272/j.issn.2095-8137.2020.006

First genetic assessment of brackish water polychaete Tylorrhynchus heterochaetus: mitochondrial COI sequences reveal strong genetic differentiation and population expansion in samples collected from southeast China and north Vietnam

doi: 10.24272/j.issn.2095-8137.2020.006
#Authors contributed equally to this work
Funds:  This work was supported by the Industry-AcademicResearch Cooperation Program of Academician Workstation of Guangdong Province (2013B090400017), Natural Science Foundation of Guangdong Province (2016A030307036), and Yangfan Innovative & Entrepreneurial Research Team Project for Guangdong Province (201312H10)
More Information
  • Tylorrhynchus heterochaetus is a widespread benthic polychaete worm found in coastal brackish waters of the west Pacific. It has high ecological and economic value as a biomarker of water quality and as a high-quality feed in aquaculture and fisheries and is considered a delicacy in some areas of Asia. However, it has experienced a marked reduction in recent years due to overexploitation as well as changes in the environment and climate. Here, to comprehensively understand its genetic background and thus provide insights for better conservation and utilization of this species, we assessed the genetic variability and demographic history of T. heterochaetus individuals sampled from eight locations along the coasts of southeast China and north Vietnam based on mitochondrial cytochrome c oxidase I (COI) sequences. We observed high haplotype diversity (Hd), with an average of 0.926, but relatively low nucleotide diversity (π), with a mean of 0.032 across all samples. A total of 94 polymorphic sites and 85 haplotypes were identified among 320 individuals. The pairwise genetic distances among haplotypes ranged from 0.001 to 0.067, with the high intraspecific divergence possibly reflecting geographic isolation and gene pool fragmentation. Significant genetic structures were revealed among the studied locations; specifically, the eight locations could be treated as six genetically different populations based on pairwise ΦST results (0.026–0.951, P<0.01). A significant pattern of isolation-by-distance was detected between the genetic and geographic distances (r=0.873, P=0.001). Three geographic lineages were defined based on phylogenetic tree and network analyses of COI haplotypes. AMOVA results indicated that genetic variations mainly occurred among the three lineages (89.96%). Tests of neutrality and mismatch distribution suggested that T. heterochaetus underwent recent population expansion. These results provide the first report on the genetic status of T. heterochaetus and will be valuable for the management of genetic resources and better understanding of the ecology and evolution in this species.

  • loading
  • [1]
    Avise JC. 2000. Phylogeography: the History and Formation of Species. Cambridge, MA: Harvard University Press.
    Bandelt HJ, Forster P, Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1): 37−48. doi:  10.1093/oxfordjournals.molbev.a026036
    Barrett RDH, Schluter D. 2008. Adaptation from standing genetic variation. Trends in Ecology & Evolution, 23(1): 38−44.
    Bilton DT, Paula J, Bishop JDD. 2002. Dispersal, genetic differentiation and speciation in estuarine organisms. Estuarine, Coastal and Shelf Science, 55(6): 937−952. doi:  10.1006/ecss.2002.1037
    Birky CW, Fuerst P, Maruyama T. 1989. Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics, 121(3): 613−627.
    Blank M, Bastrop R. 2009. Phylogeny of the mud worm genus Marenzelleria (Polychaeta, Spionidae) inferred from mitochondrial DNA sequences. Zoologica Scripta, 38(3): 313−321. doi:  10.1111/j.1463-6409.2008.00370.x
    Chen X, Li M, Liu H, Li B, Guo L, Meng Z, Lin H. 2016. Mitochondrial genome of the polychaete Tylorrhynchus heterochaetus (Phyllodocida, Nereididae). Mitochondrial DNA Part A, 27(5): 3372−3373. doi:  10.3109/19401736.2015.1018226
    Costa PFE, Gil J, Passos A M, Pereira P, Melo P, Batista F, Da Fonseca LC. 2006. The market features of imported non-indigenous polychaetes in Portugal and consequent ecological concerns. Scientia Marina, 70(S3): 287−292. doi:  10.3989/scimar.2006.70s3287
    Cowen RK, Sponaugle S. 2009. Larval dispersal and marine population connectivity. Annual Review of Marine Science, 1: 443−466. doi:  10.1146/annurev.marine.010908.163757
    Darling JA, Reitzel AM, Finnerty JR. 2004. Regional population structure of a widely introduced estuarine invertebrate: Nematostella vectensis Stephenson in New England. Molecular Ecology, 13(10): 2969−2981. doi:  10.1111/j.1365-294X.2004.02313.x
    Dean HK. 2008. The use of polychaetes (Annelida) as indicator species of marine pollution: a review. Revista de Biologia Tropical, 56(4): 11−38.
    Duan XH, Liu WS, Xu AY, Xu CH, He QT, Xiao RY, Pan G. 2017. Observation on embryonic development of Tylorrhynchus heterochaeta and effect of salinity on their hatching. South China Fisheries Science, 13(4): 115−121.
    Excoffier L, Layal G, Schneider S. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics, 1: 47−50.
    Fairbanks RG. 1989. A 17, 000-year glacio-eustatic sea level record: influence of glacial melting rates on the Younger Dryas event and deepocean circulation. Nature, 342(6250): 637−642. doi:  10.1038/342637a0
    Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3(5): 294−299.
    Fu YX. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147(2): 915−925.
    Gao X, Mu D, Lou J, Hou C, Zhu J, Wang J, Jin S. 2018. Genetic diversity and structure analysis of Phascolosoma esculenta in the coastal zone of south-eastern China based on mitochondrial Cyt b gene. Turkish Journal of Fisheries and Aquatic Sciences, 18(4): 519−528.
    Glasby CJ, Timm T. 2008. Global diversity of polychaetes (Polychaeta; Annelida) in freshwater. Hydrobiologia, 595: 107−115. doi:  10.1007/s10750-007-9008-2
    Grant WAS, Bowen BW. 1998. Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. Journal of Heredity, 89(5): 415−426. doi:  10.1093/jhered/89.5.415
    Green BN, Suzuki T, Gotoh T, Kuchumov AR, Vinogradov SN. 1995. Electrospray ionization mass spectrometric determination of the complete polypeptide chain composition of Tylorrhynchus heterochaetus hemoglobin. Journal of Biological Chemistry, 270(31): 18209−18211. doi:  10.1074/jbc.270.31.18209
    Harpending H. 1994. Signature of ancient population growth in a lowresolution mitochondrial DNA mismatch distribution. Human Biology, 66(4): 591−600.
    Hebert PDN, Ratnasingham S, de Waard JR. 2003. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270(S1): S96−S99.
    Imbrie J, Boyle EA, Clemens SC, Duffy A, Howard WR, Kukla G, Kutzbach J, Martinson DG, McIntyre A, Mix AC, Molfino B, Morley JJ, Peterson LC, Pisias NG, Prell WL, Raymo ME, Shackleton NJ, Toggweiler JR. 1992. On the structure and origin of major glaciation cycles 1. Linear responses to Milankovitch forcing. Paleoceanography and Paleoceanography, 7(6): 701−738. doi:  10.1029/92PA02253
    Jolly MT, Viard F, Gentil F, Thiébaut É, Jollivet D. 2006. Comparative phylogeography of two coastal polychaete tubeworms in the Northeast Atlantic supports shared history and vicariant events. Molecular Ecology, 15(7): 1841−1855. doi:  10.1111/j.1365-294X.2006.02910.x
    Kaoawa Y. 1954. Histological Observations on the transformation to mature worms of Tylorrhynchus heterochaetus. Journal of Gakugei, Tokushima University, 4: 65−71.
    Kesäniemi JE, Rawson PD, Lindsay SM, Knott KE. 2012. Phylogenetic analysis of cryptic speciation in the polychaete Pygospio elegans. Ecology and Evolution, 2(5): 994−1007. doi:  10.1002/ece3.226
    Koizumi I, Tada R, Narita H, Irino T, Aramaki T, Oba T, Yamamoto H. 2006. Paleoceanographic history around the Tsugaru Strait between the Japan Sea and the Northwest Pacific Ocean since 30 cal kyr BP. Palaeogeography, Palaeoclimatology, Palaeoecology, 232(1): 36−52. doi:  10.1016/j.palaeo.2005.09.003
    Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version7.0 for bigger datasets. Molecular Biology and Evolution, 33(7): 1870−1874. doi:  10.1093/molbev/msw054
    Kyle CJ, Boulding EG. 2000. Comparative population genetic structure of marine gastropods (Littorina spp.) with and without pelagic larval dispersal. Marine Biology, 137(5-6): 835−845. doi:  10.1007/s002270000412
    Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25(11): 1451−1452. doi:  10.1093/bioinformatics/btp187
    Liu F, Guo QS, Shi HZ, Lv F, Yu YB, Lv LL. Huang JT, Wang AM, Liang HX. 2014. Genetic diversity analysis of Perinereis aibuhitensis based on ISSR and SRAP markers of Chinese coast populations. Biochemical Systematics and Ecology, 57: 262−269. doi:  10.1016/j.bse.2014.08.025
    Liu H, Liu M, Ge S, Wang Q, Yu D, Guan S. 2012. Population structuring and historical demography of a common clam worm Perinereris aibuhitensis, near the coasts of Shandong Peninsula. Biochemical Systematics and Ecology, 44(4): 70−78.
    Loeschcke V, Tomiuk J, Jain SK. 2013. Conservation genetics (Vol. 68. Basel: Birkhäuser, 37-53.
    Méndez N, Linke-Gamenick I, Forbes VE, Baird DJ. 2001. Sediment processing in Capitella spp. (Polychaeta: Capitellidae): strain-specific differences and effects of the organic toxicant fluoranthene. Marine Biology, 138(2): 311−319. doi:  10.1007/s002270000440
    Okada K. 1952. Experimental studies on the Japanese palolo, Tylorrhynchus heterochaetus. I. activation of egg-cells. Journal of Gakugei, Tokushima University, 2: 43−52.
    Olson MA, Zajac RN, Russello MA. 2009. Estuarine-scale genetic variation in the polychaete Hobsonia florida (Ampharetidae; Annelida) in Long Island Sound and relationships to Pleistocene glaciations. The Biological Bulletin, 217(1): 86−94. doi:  10.1086/BBLv217n1p86
    Pinsky ML, Palumbi SR. 2014. Meta-analysis reveals lower genetic diversity in overfished populations. Molecular Ecology, 23(1): 29−39. doi:  10.1111/mec.12509
    Plouviez S, Shank TM, Faure B, Daguin-Thiebaut C, Viard F, Lallier FH, Jollivet D. 2009. Comparative phylogeography among hydrothermal vent species along the East Pacific Rise reveals vicariant processes and population expansion in the South. Molecular Ecology, 18(18): 3903−3917. doi:  10.1111/j.1365-294X.2009.04325.x
    Provan J, Bennett KD. 2008. Phylogeographic insights into cryptic glacial refugia. Trends in Ecology & Evolution, 23(10): 564−571.
    Rogers AR, Harpending H. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9(3): 552−569.
    Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4): 406−425.
    Sato M, Osanai K. 1990. Sperm attachment and acrosome reaction on the egg surface of the polychaete, Tylorrhynchus heterochaetus. The Biological Bulletin, 178(2): 101−110. doi:  10.2307/1541968
    Selkoe KS, Toonen RJ. 2011. Marine connectivity: a new look at pelagic larval duration and genetic metrics of dispersal. Marine Ecology Progress Series, 436: 291−305. doi:  10.3354/meps09238
    Simon CA, Sato-Okoshi W. 2015. Polydorid polychaetes on farmed molluscs: distribution, spread and factors contributing to their success. Aquaculture Environment Interactions, 7(2): 147−166. doi:  10.3354/aei00138
    Slatkin M, Hudson RR. 1991. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics, 129(2): 555−562.
    Smith LM, Hutchings P, Fraser CI. 2015. Molecular evidence supports coastal dispersal among estuaries for two benthic marine worm (Nephtyidae) species in southeastern Australia. Marine Biology, 162(6): 1319−1327. doi:  10.1007/s00227-015-2671-3
    Suzuki T, Gotoh T. 1986. The complete amino acid sequence of giant multisubunit hemoglobin from the polychaete Tylorrhynchus heterochaetus. Journal of Biological Chemistry, 261(20): 9257−9267.
    Suzuki T, Takagi T, Gotoh T. 1990. Primary structure of two linker chains of the extracellular hemoglobin from the polychaete Tylorrhynchus heterochaetus. Journal of Biological Chemistry, 265(21): 12168−12177.
    Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123(3): 585−595.
    Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25(24): 4876−4882. doi:  10.1093/nar/25.24.4876
    Tuan NN. 2018. Biological characteristics and effects of salinity on reproductive activities of marine worm (Tylorrhynchus heterochaetus, Quatefages, 1865) in summer season in Hai Phong - Viet Nam. SNRU Journal of Science and Technology, 10(1): 25−31.
    Virgilio M, Backeljau T, Abbiati M. 2006. Mitochondrial DNA and allozyme patterns of Hediste diversicolor (Polychaeta: Nereididae): the importance of small scale genetic structuring. Marine Ecology Progress Series, 326: 157−165. doi:  10.3354/meps326157
    Voris HK. 2000. Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography, 27(5): 1153−1167. doi:  10.1046/j.1365-2699.2000.00489.x
    Weersing K, Toonen RJ. 2009. Population genetics, larval dispersal, and connectivity in marine systems. Marine Ecology Progress Series, 393: 1−12. doi:  10.3354/meps08287
    Whiteley AR, Spruell P, Allendorf FW. 2006. Can common species provide valuable information for conservation?. Molecular Ecology, 15(10): 2767−2786. doi:  10.1111/j.1365-294X.2006.02972.x
    Zakas C, Wares JP. 2012. Consequences of a poecilogonous life history for genetic structure in coastal populations of the polychaete Streblospio benedicti. Molecular Ecology, 21(22): 5447−5460. doi:  10.1111/mec.12040
    Zardi GI, McQuaid CD, Teske PR, Teske PR, Barker NP. 2007. Unexpected genetic structure of mussel populations in South Africa: indigenous Perna perna and invasive Mytilus galloprovincialis. Marine Ecology Progress Series, 337: 135−144. doi:  10.3354/meps337135
  • Relative Articles

    [1] Zhong-Yuan Shen, Dan Yu, Xin Gao, Fu-Tie Zhang, Huan-Zhang Liu. Genetic diversity and reproductive success of a wild population of Chinese sturgeon (Acipenser sinensis) from the Yangtze River inferred from juveniles born in 2014. Zoological Research, 2020, 41(4): 423-430.  doi: 10.24272/j.issn.2095-8137.2020.011
    [2] Zong-Ji Wang, Guang-Ji Chen, Guo-Jie Zhang, Qi Zhou. Dynamic evolution of transposable elements, demographic history, and gene content of paleognathous birds. Zoological Research, 2020, 41(6): 1-11.  doi: 10.24272/j.issn.2095-8137.2020.175
    [3] Dong-Dong Zhai, Wen-Jing Li, Huan-Zhang Liu, Wen-Xuan Cao, Xin Gao. Genetic diversity and temporal changes of an endemic cyprinid fish species, Ancherythroculter nigrocauda, from the upper reaches of Yangtze River. Zoological Research, 2019, 40(5): 427-438.  doi: 10.24272/j.issn.2095-8137.2019.027
    [4] Jing Yang, Guo-Fen Zhu, Jian Jiang, Chang-Lin Xiang, Fu-Li Gao, Wei-Dong Bao. Non-invasive genetic analysis indicates low population connectivity in vulnerable Chinese gorals: concerns for segregated population management. Zoological Research, 2019, 40(5): 439-448.  doi: 10.24272/j.issn.2095-8137.2019.058
    [5] Jin-Jin MIN, Rong-Hui YE, Gen-Fang ZHANG, Rong-Quan ZHENG. Microsatellite analysis of genetic diversity and population structure of freshwater mussel (Lamprotula leai). Zoological Research, 2015, 36(1): 34-40.  doi: 10.13918/j.issn.2095-8137.2015.1.34
    [6] Ya HE, Zheng-Huan WANG, Xiao-Ming WANG. Genetic diversity and population structure of a Sichuan sika deer (Cervus sichuanicus) population in Tiebu Nature Reserve based on microsatellite variation. Zoological Research, 2014, 35(6): 528-536.  doi: 10.13918/j.issn.2095-8137.2014.6.528
    [7] Xing-Jian YUE, Shao-Ping LIU, Ming-Dian LIU, Xin-Bin DUAN, Deng-Qiang WANG, Da-Qing CHEN. Age structure and genetic diversity of Homatula pycnolepis in the Nujiang River basin. Zoological Research, 2013, 34(4): 392-398.  doi: 10.11813/j.issn.0254-5853.2013.4.0392
    [8] ZHENG Wen-Juan, LAI Yu-Hong, YOU Xin-Yu, QIN Xi-Han, ZHU Shi-Hua. Genetic diversity of Pseudosciaena polyactis in Zhoushan based on mitochondrial DNA D-loop region sequences. Zoological Research, 2012, 33(3): 329-336.  doi: 10.3724/SP.J.1141.2012.03329
    [9] Zhiying JIA, Yuyong ZHANG, Shuqiang CHEN, Lianyu SHI. Genetic diversity and differentiation of masu salmon (Oncorhynchus masou masou) between and within cultured populations inferred from microsatellite DNA analysis. Zoological Research, 2012, 33(E3-4): 33-39.  doi: 10.3724/SP.J.1141.2012.E03-04E33
    [10] CHEN Shi-Yi, XU Ling, Lü Long-Bao, YAO Yong-Gang. Genetic diversity and matrilineal structure in Chinese tree shrews inhabiting Kunming, China. Zoological Research, 2011, 32(1): 17-23.  doi: 10.3724/SP.J.1141.2011.01017
    [11] LI Ou, ZHAO Ying-ying, GUO Na, LU Cui-yun, SUN Xiao-wen. Effects of Sample Size and Loci Number on Genetic Diversity in Wild Population of Grass Carp Revealed by SSR. Zoological Research, 2009, 30(2): 121-130.  doi: 10.3724/SP.J.1141.2009.02121
    [12] QI De-lin. Genetic Variation and Diversity of Gymncypris eckloni in the Upper Yellow River Inferred from Mitochondrial Cytochrome b Gene. Zoological Research, 2009, 30(3): 255-261.  doi: 10.3724/SP.J.1141.2009.03255
    [13] LIU Yan-hua, ZHANG Ming-hai. Population Genetic Diversity of Roe Deer (Capreolus pygargus) in Mountains of Heilongjiang Province. Zoological Research, 2009, 30(2): 113-120.  doi: 10.3724/SP.J.1141.2009.02113
    [14] YANG Bo, CHEN Xiao-yong, YANG Jun-xing. Structure of the Mitochondrial DNA Control Region and Population Genetic Diversity Analysis of Anabarilius grahami (Regan). Zoological Research, 2008, 29(4): 379-385.  doi: 10.3724/SP.J.1141.2008.04379
    [15] ZHU Shi-hua, ZHENG Wen-juan, ZOU Ji-xing, YANG Ying-chun, SHEN Xi-quan. Mitochondrial DNA Control Region Structure and MolecularPhylogenetic Relationship of Carangidae. Zoological Research, 2007, 28(6): 606-614.
    [16] YE Lang-hui HUO Jin-long MIAO Yong-wang , * ZHU Sheng-quan CHEN Tao LIU Li-xian PAN Wei-rong BI Bao-liang. Genetic Diversity Analysis of Nixi Chicken Using Microsatellite DNA Markers. Zoological Research, 2006, 27(1): 68-74.
    [17] ZHOU Li, LIU Jin-Xia, GUI Jian-Fang. Preliminary Investigation on Genetic Diversity of Gynogenetic Silver Crucian Carp (Carassius auratus gibelio Bloch) Detected by Microsatellite DNA. Zoological Research, 2001, 22(4): 257-264.
    [18] ZHUANG Zhi-meng, MENG Xian-hong, QUAN Jie-xia, DAI Ji-xun, DENG Jing-yao. Genetic Diversity in The Wild Population and Hatchery Stock of Penaeus japonicus Shrimp by Isoenzyme Analysis. Zoological Research, 2000, 21(4): 323-326.
    [19] ZHANG Sheng-qiao, XU Ji-chu, ZHANG Ya-ping, FU Yan, CHEN Yong-jiu. Genetic Diversity of Zhejiang Native Pig Breeds Inferred From Mitochondrial DNA Polymorphism. Zoological Research, 1998, 19(2): 125-130.
    [20] LI Xiang-long, ZHANG Ya-ping, CHEN Shen-gou, ZENG Fan-tong, QIU Xiang-pin, LIU Xiang-mo. Study on The mtDNA Rflp of Goat Breeds. Zoological Research, 1997, 18(4): 421-428.
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(3)  / Tables(5)

    Article Metrics

    Article views (1779) PDF downloads(366) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint