Skip to main content
Log in

Microsatellite markers for the Ussuri white-toothed shrew (Soricidae: Crocidura lasiura) developed by Ion Torrent sequencing and their application to the shrew populations in disturbed forests

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

Understanding the impacts of forest management practices on genetic diversity is essential for effective animal management and conservation. We characterized novel microsatellite loci in the Ussuri white-toothed shrew (Crocidura lasiura Dobson, 1890) to test the impacts of anthropogenic thinning of forest trees on the shrew populations and their genetic diversity. Using Ion Torrent sequencing technology, we characterized 611 potential microsatellite markers with complete di- to tetra-nucleotide motifs, identifying nine polymorphic loci. The observed and expected heterozygosities across the nine loci were 0.526 and 0.527, respectively. Mean allelic diversity was 5.2 alleles per locus, with the mean polymorphism information content at 0.498. In comparison among shrew populations, which inhabited in the forests thinned in 2004 (CLA; n = 10), 2008 (CLB; n = 9) and 2014 (CLC; n = 3), the observed heterozygosities are similar among the three populations (0.525 at CLA, 0.532 at CLB and 0.519 at CLC), whereas the expected heterozygosities were much lower in population of CLC (0.377) than that of CLA (0.509) and CLB (0.533). The small sample size at CLC limited effective comparison and evaluation of the impact of forest thinning on genetic diversity in this shrew population. Future application of the species-specific microsatellite markers described here to a larger sample size would be valuable in estimating the ecological parameters of shrew populations associated with existing forest management practices.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Alfaro RI, Fady B, Vendramin GG, Dawson IK, Fleming RA, Saenz-Romero C, Lindig-Cisneros RA, Murdock T, Vinceti B, Navarro CM et al (2014) The role of forest genetic resources in responding to biotic and abiotic factors in the context of anthropogenic climate change. For Ecol Manag 333:76–87

    Article  Google Scholar 

  • Calmet C, Lambourdiere J, Abdelkrim J, Pascal M, Samadi S (2004) Characterization of eight polymorphic microsatellites in the shrew Crocidura suaveolens and its application to the study of insular populations of the French Atlantic coast. Mol Ecol Notes 4:426–428

    Article  CAS  Google Scholar 

  • Dickman C (1995) Diets and habitat preferences of three species of Crocidurine shrews in arid southern Africa. J Zool 237:499–513

    Article  Google Scholar 

  • El-Kassaby Y, Dunsworth B, Krakowski J (2003) Genetic evaluation of alternative silvicultural systems in coastal montane forests: western hemlock and amabilis fir. Theor Appl Genet 107:598–610

    Article  CAS  PubMed  Google Scholar 

  • Elliott CP, Enright NJ, Allcock RJN, Gardner MG, Meglecz E, Anthony J, Krauss S (2014) Microsatellite markers from the Ion Torrent: a multi-species contrast to 454 shotgun sequencing. Mol Ecol Resour 14:554–568

    Article  CAS  PubMed  Google Scholar 

  • Eo SH, Lee WS, Glenn TC, Jones K, Lee EJ, Park YS, Carroll JP, Rhim SJ (2009) Development of polymorphic microsatellite DNA markers from the Korean field mouse, Apodemus peninsulae. Conserv Genet 10:1923–1925

    Article  CAS  Google Scholar 

  • Eo SH, Doyle J, DeWoody J (2011a) Genetic diversity in birds is associated with body mass and habitat type. J Zool 283:220–226

    Article  Google Scholar 

  • Eo SH, Rhim S, Lee W, Carroll JP (2011b) Genetic diversity and population structure of the Korean field mouse (Apodumus peninsulae) in South Korea: from 17 previously and newly developed microsatellite markers. Genes Genomics 33:445–449

    Article  Google Scholar 

  • Faircloth BC (2008) msatcommander: detection of microsatellite repeat arrays and automated, locus-specific primer design. Mol Ecol Resour 8:92–94

    Article  CAS  PubMed  Google Scholar 

  • Gardner MG, Fitch AJ, Bertozzi T, Lowe AJ (2011) Rise of the machines–recommendations for ecologists when using next generation sequencing for microsatellite development. Mol Ecol Resour 11:1093–1101

    Article  PubMed  Google Scholar 

  • Glenn TC (2011) Field guide to next-generation DNA sequencers. Mol Ecol Resour 11:759–769

    Article  CAS  PubMed  Google Scholar 

  • Glenn T, Schable N (2005) Isolating microsatellite DNA loci. Methods Enzymol 395:202–222

    Article  CAS  PubMed  Google Scholar 

  • Igawa T, Nozawa M, Nagaoka M, Komaki S, Oumi S, Fujii T, Sumida M (2015) Microsatellite marker development by multiplex Ion Torrent PGM sequencing: a case study of the endangered Odorrana narina complex of frogs. J Hered 106:131–137

    Article  PubMed  Google Scholar 

  • Jeong S, Yoon M (2001) Spermatogenesis in three Korean shrews and notes on their phylogenetic significance. Korean J Life Sci 11:218–229

    Google Scholar 

  • Kim H, Kang M (1997) A morphological analysis of external and cranial characters of big white toothed shrews (Crocidura lasiura) in Korea. Korean J Vet Public Health 21:33–40

    Google Scholar 

  • Kwon GH (2014) Systematics and conservation on three species (Crocidura lasiura, Crocidura shantungensis, Sorex caecutiens) of family Soricidae based on DNA sequence analyses. PhD Dissertation, Chungbuk National University

  • Ledig FT (1992) Human impacts on genetic diversity in forest ecosystems. Oikos 63:87–108

    Article  Google Scholar 

  • Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129

    Article  CAS  PubMed  Google Scholar 

  • Luo W, Nie Z, Zhan F, Wei J, Wang W, Gao Z (2012) Rapid development of microsatellite markers for the endangered fish Schizothorax biddulphi (Günther) using next generation sequencing and cross-species amplification. Int J Mol Sci 13:14946–14955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Motokawa M, Yu H, Harada M (2005) Diversification of the white-toothed shrews of the genus Crocidura (Insectivora: Soricidae) in East and Southeast Asia. Mammal Study 30:S53–S64

    Article  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ratnam W, Rajora OP, Finkeldey R, Aravanopoulos F, Bouvet JM, Vaillancourt RE, Kanashiro M, Fady B, Tomita M, Vinson C (2014) Genetic effects of forest management practices: global synthesis and perspectives. For Ecol Manag 333:52–65

    Article  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

    Article  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa

    Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotech 18:233–234

    Article  CAS  Google Scholar 

  • Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629

    Article  PubMed  Google Scholar 

  • Steffens DL, Sutter SL, Roemer SC (1993) An alternate universal forward primer for improved automated DNA sequencing of M13. Biotechniques 15:580–582

    CAS  PubMed  Google Scholar 

  • Tsytsulina K (2008) Crocidura lasiura. The IUCN Red List of Threatened Species. Version 2015.2. www.iucnredlist.org. Accessed 03 July 2015

  • Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Wilson DE, Reeder DM (2005) Mammal Species of the World. In: A taxonomic and geographic reference (3rd ed) Johns Hopkins University Press, Baltimore

  • Yoon M, Jeong S (2001) Ultrastructure of epididymal spermatozoa in three Korean shrews. Korean J Life Sci 11:54–61

    Google Scholar 

  • Yu J, Won C, Jun J, Lim Y, Kwak M (2011) Fast and cost-effective mining of microsatellite markers using NGS technology: an example of a Korean water deer Hydropotes inermis argyropus. Plos One 6:e26933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We appreciate valuable comments on the manuscript by an anonymous reviewer. This study was carried out with the support of ‘R&D Program for Forestry Technology (Project Nos. S211315L020120 and S211315L020130)’ provided by Korea Forest Service.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Soo Hyung Eo.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

All animal experiments throughout the study were conducted in accordance with guidelines of Kongju National University for the care and use of animals.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eo, S.H., Lee, WS., Lee, BJ. et al. Microsatellite markers for the Ussuri white-toothed shrew (Soricidae: Crocidura lasiura) developed by Ion Torrent sequencing and their application to the shrew populations in disturbed forests. Genes Genom 38, 351–357 (2016). https://doi.org/10.1007/s13258-015-0375-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-015-0375-1

Keywords