Skip to main content
SpringerLink
Log in

Assessment of the genetic relationship between the recently established benthic population and the adjacent floating populations of Sargassum horneri (Phaeophyceae) in Dalian of China by newly developed trinucleotide microsatellite markers

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Sargassum horneri is a conspicuous canopy-forming brown seaweed growing on solid substrates or floating on sea surface. A recently established benthic population was discovered in a bay in Dalian, China, in 2016 and suggested to be derived from the earlier floating population. Since 2016, floating populations have kept appearing in the adjacent area. The genetic connectivity between this recently established benthic population and the adjacent floating populations remains unclear. In this study, 10 novel informative trinucleotide microsatellite markers were developed through the high throughput sequencing technology, and employed to analyze the genetic structure of the benthic population (DS16 and DS18) and three adjacent floating populations (DL16, BL16, and DL18) sampled in 2016 and 2018, with one floating population collected from Shidao in 2016 (SD16) as reference. Significant genetic differentiation was found to exist between the benthic and floating populations, and among floating populations from different years. Almost no membership of floating populations was detected in the benthic population and vice versa by the Bayesian model–based structure analysis, indicating very limited genetic connectivity between them. Significant excess of heterozygosity, significant multilocus linkage disequilibrium, high frequency of repeated genotypes, and putative clones were detected in all floating populations, indicating that asexual reproduction is likely dominant in them. Inbreeding and founder effect were revealed to be present in the benthic population. Further studies will focus on tracking the dynamics of genetic structure in the recently established benthic population and investigating the exact reproductive means and patterns of floating populations.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agapow PM, Burt A (2010) Indices of multilocus linkage disequilibrium. Mol Ecol Notes 1:101–102

    Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289–300

    Google Scholar 

  • Critchley AT, Farnham WF, Morrell SL (1983) A chronology of new European sites of attachment for the invasive brown alga, Sargassum muticum, 1973–1981. J Mar Biol Assoc UK 63:799–811

    Google Scholar 

  • David P, Pujol B, Viard F, Castella V, Goudet J (2007) Reliable selfing rate estimates from imperfect population genetic data. Mol Ecol 16:2474–2487

    CAS  PubMed  Google Scholar 

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

    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

    CAS  PubMed  Google Scholar 

  • Fraser CI, Thiel M, Spencer HG, Waters JM (2010) Contemporary habitat discontinuity and historic glacial ice drive genetic divergence in Chilean kelp. BMC Evol Biol 10:203

    PubMed  PubMed Central  Google Scholar 

  • Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O, Lepoittevin C, Malausa T, Revardel E, Salin F (2011) Current trends in microsatellite genotyping. Mol Ecol Resour 11:591–611

    CAS  PubMed  Google Scholar 

  • Guillemin ML, Faugeron S, Destombe C, Viard F, Correa JA, Valero M (2008) Genetic variation in wild and cultivated populations of the haploid-diploid red alga Gracilaria chilensis: how farming practices favor asexual reproduction and heterozygosity. Evolution 62:1500–1519

    PubMed  Google Scholar 

  • Hobday AJ (2000) Abundance and dispersal of drifting kelp Macrocystis pyrifera rafts in the Southern California Bight. Mar Ecol Prog Ser 195:101–116

    Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    PubMed  PubMed Central  Google Scholar 

  • Komatsu T, Ariyama H, Nakahara H, Sakamoto W (1982) Spatial and temporal distributions of water temperature in a Sargassum forest. J Oceanogr Soc Jpn 38:63–72

    Google Scholar 

  • Komatsu T, Tatsukawa K, Filippi JB, Sagawa T, Matsunaga D, Mikami A, Ishida K, Ajisaka T, Tanaka K, Aoki M, Wang W-D, Liu H-F, Zhang S-D, Zhou M-D, Sugimoto T (2007) Distribution of drifting seaweeds in eastern East China Sea. J Mar Syst 67:245–252

    Google Scholar 

  • Kubo N, Douke A, Nishigaki T, Tsuji G (2017) Development and characterization of simple sequence repeat markers for genetic analyses of Sargassum horneri (Sargassaceae, Phaeophyta) populations in Kyoto, Japan. J Appl Phycol 29:1729–1733

    CAS  Google Scholar 

  • Laurent E, Guillaume L, Stefan S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47–50

    Google Scholar 

  • Li Q, Zhang J, Yao J, Wang X, Duan D (2016) Development of Saccharina japonica genomic SSR markers using next-generation sequencing. J Appl Phycol 28:1387–1390

    CAS  Google Scholar 

  • Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:18–18

    PubMed  PubMed Central  Google Scholar 

  • Macaya EC, Boltana S, Hinojosa IA, Macchiavello JE, Valdivia NA, Vasquez NR, Buschmann AH, Vasquez JA, Alonso Vega JM, Thiel M (2005) Presence of sporophylls in floating kelp rafts of Macrocystis spp. (Phaeophyceae) along the Chilean Pacific coast. J Phycol 41:913–922

    Google Scholar 

  • Meeûs TD, Balloux F (2004) Clonal reproduction and linkage disequilibrium in diploids: a simulation study. Infect Genet Evol 4:345–351

    PubMed  Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Google Scholar 

  • Pang SJ, Liu F, Shan TF, Gao SQ, Zhang ZH (2009) Cultivation of the brown alga Sargassum horneri: sexual reproduction and seedling production in tank culture under reduced solar irradiance in ambient temperature. J Appl Phycol 21:413–422

    Google Scholar 

  • Peakall R, Smouse PE (2006) genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Resour 6:288–295

    Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Google Scholar 

  • Rousset F (2008) GENEPOP'007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365

    CAS  PubMed  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Google Scholar 

  • Shan T, Pang S, Li J, Su L (2015) Isolation and characterization of eight novel microsatellite loci from the brown alga Sargassum horneri. J Appl Phycol 27:2419–2421

    CAS  Google Scholar 

  • Shan T, Yotsukura N, Pang S (2017) Novel implications on the genetic structure of representative populations of Saccharina japonica (Phaeophyceae) in the Northwest Pacific as revealed by highly polymorphic microsatellite markers. J Appl Phycol 29:631–638

    Google Scholar 

  • Shan T, Pang S, Wang X, Li J, Su L (2018) Assessment of the genetic connectivity between farmed and wild populations of Undaria pinnatifida (Phaeophyceae) in a representative traditional farming region of China by using newly developed microsatellite markers. J Appl Phycol 30:2707–2714

    Google Scholar 

  • Stoeckel S, Grange J, Fernandez-Manjarres J, Bilger I, Frascaria-Lacoste N (2010) Heterozygote excess in a self-incompatible and partially clonal forest tree species - Prunus avium L. Mol Ecol 15:2109–2118

    Google Scholar 

  • Stoffel MA, Esser M, Kardos M, Humble E, Nichols H, David P, Hoffman JI, Poisot T (2016) inbreedR: an R package for the analysis of inbreeding based on genetic markers. Methods Ecol Evol 7 (11):1331–1339

    Google Scholar 

  • Su L, Shan T, Pang S, Li J (2018) Analyses of the genetic structure of Sargassum horneri in the Yellow Sea: implications of the temporal and spatial relations among floating and benthic populations. J Appl Phycol 30:1417–1424

    Google Scholar 

  • Sun J, Chen W, Zhuang D, Zheng H, Lin L, Pang S (2008) In situ ecological studies of the subtidal brown alga Sargassum horneri at Nanji Island of China. S China Fish Sci 4:59–64 (in Chinese with English abstract)

    Google Scholar 

  • Takezaki N, Nei M, Tamura K (2010) POPTREE2: software for constructing population trees from allele frequency data and computing other population statistics with Windows interface. Mol Biol Evol 27:747–752

    CAS  PubMed  Google Scholar 

  • Thiel M, Gutow L (2005) The ecology of rafting in the marine environment. I. The floating substrata. Oceanogr Mar Biol 42:181–264

    Google Scholar 

  • Tseng CK (2000) Flora Algarum Marinarum Sinicarum, Tomus 3. Phaeophyta (no. 2). Fucales. Science Press, Beijing (in Chinese)

  • Uchida T, Arima S (1993) Crossing experiments between autumn-and spring-fruiting types of Sargassum horneri (Phaeophyta). Nippon Suisan Gakkaishi 59:1685–1688

    Google Scholar 

  • Waters JM, Fraser CI, Hewitt GM (2013) Founder takes all: density-dependent processes structure biodiversity. Trends Ecol Evol 28:78–85

    PubMed  Google Scholar 

  • Yoshida G, Yoshikawa K, Terawaki T (2001) Growth and maturation of two populations of Sargassum horneri (Fucales, Phaeophyta) in Hiroshima Bay, the Seto Inland Sea. Fish Sci 67:1023–1029

    Google Scholar 

  • Zhang L, Peng J, Li X, Liu Y, Cui C, Wu H, Wu R, Tian P, Li Y (2014) Development of 27 trinucleotide microsatellite markers for Saccharina japonica using next generation sequencing technology. Conserv Genet Resour 6:341–344

    CAS  Google Scholar 

Download references

Funding

This research was supported by grants from the State’s Key Project of Research and Development Plan (2016YFC1402507), National Key Technology Support Program (2015BAD13B05), China Agriculture Research System (CARS-50), the Taishan Scholar Program of Shandong Province, and the Foundation for Huiquan Scholar of Institute of Oceanology, Chinese Academy of Sciences.

Author information

Authors and Affiliations

  1. CAS Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai Rd., Qingdao, 266071, China

    Xuemei Wang, Tifeng Shan, Shaojun Pang & Li Su

  2. Center for Ocean Mega-Science, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao, 266071, People’s Republic of China

    Xuemei Wang, Tifeng Shan, Shaojun Pang & Li Su

  3. Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, 7 Nanhai Rd., Qingdao, 266071, China

    Xuemei Wang, Tifeng Shan, Shaojun Pang & Li Su

  4. University of Chinese Academy of Sciences, Beijing, 100049, China

    Xuemei Wang

Authors
  1. Xuemei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tifeng Shan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shaojun Pang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Li Su
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S. Pang and T. Shan conceived the study; X. Wang and L. Su performed DNA isolation and PCR work. X. Wang and T. Shan performed genotyping and genetic analysis. Everyone contributed to the sample collection and manuscript writing.

Corresponding authors

Correspondence to Tifeng Shan or Shaojun Pang.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Table S1

Genetic diversity of the six populations of Sargassum horneri. (DOCX 24.5 kb)

Table S2

Number of genotypes, putative clones, and individuals included in putative clones in 12 floating populations of Sargassum horneri (Su et al. 2018). (DOCX 14.9 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Shan, T., Pang, S. et al. Assessment of the genetic relationship between the recently established benthic population and the adjacent floating populations of Sargassum horneri (Phaeophyceae) in Dalian of China by newly developed trinucleotide microsatellite markers. J Appl Phycol 31, 3989–3996 (2019). https://doi.org/10.1007/s10811-019-01853-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-019-01853-2

Keywords

Search

Navigation